PLoSWiki wiki http://topicpageswiki.plos.org/wiki/Main_Page MediaWiki 1.32.1 first-letter Media Special Talk User User talk PLoSWiki PLoSWiki talk File File talk MediaWiki MediaWiki talk Template Template talk Help Help talk Category Category talk Module Module talk 0 741 7357 2019-03-05T10:38:35Z Annarunemark 132 Created page with "{{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund,..." wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Hybridization is the process where genetically closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is an important source of novel variation. Although most hybrids are sterile or less fit than their parents, some may be survive and reproduce and enable the transfer of adaptive variants across the species boundary, or even result in the formation of novel lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number. Homoploid hybrids can sort the intrinsic barriers that isolate the parent species from each other so that a subset of these isolate the hybrid species against each parent species, or gain pre-mating extrinsic isolation from ecological differences. Hybrid species may face problems arising from incompatible combinations of genes derived from different parent species. During the process of genome stabilization selection for compatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. ==Background== Genetic exchange between species can impede biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed hybridization as maladaptive sexual preferences [2] which resulted in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary force in animals [1,6,7]. Hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species [1]. Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches [8], African ''Haplochromis'' cichlid fishes [9], ''Heliconius'' butterflies [10-12] and Hawaiian ''Madiinae'' tarweeds and silverswords [13]. Here we review the evolutionary outcomes of hybridization and the properties of genomes of hybrid species. ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If hybrids are not viable or sterile, hybridization will not affect the parent species, except perhaps for a reduction in their reproductive success [14,15]. In contrast, if the fitness of hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [16,17]; Fig. 1). If the fitness of hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [18]. Hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct in spite of occassional gene flow [19,20]. In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [21,22]. Below we describe the evolutionary outcomes of hybridisation that result in hybrid genomes. [[File:Figure1 Potential evolutionary outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental specis can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from the mosquito ''Anopheles gambiae'' to ''A. coluzzii'' [20] and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta'' [23] and other ''Heliconius'' species [19]. In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from ''A. lyrata'' [24]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [25]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., a hybrid species [1,21]. A hybrid species has an admixed genome and forms stable genetically distinct populations [21]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion of a hybrid species [26], but see [27]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied homoploid hybrid species e.g. the butterfly ''Heliconius heurippa'' [10-12], the Italian sparrow ''Passer italiae'' [28], and three ''Helianthus'' sunflower species [29] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [26]. Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (introgressive speciation, c.f. [30]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinatorial hybrid speciation, [21]). A recombinatorial hybrid taxon typically also has a substantial proportion of the genome derived from the minority parent, although variation exist both between taxa and within lineages of hybrid taxa, see e.g. [31,32]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [27,29,33-37]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in increased ploidy compared to their parental taxa (Fig. 2). This form of hybrid speciation is more common in plants than in animals [38]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [38], but reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. [[File:Figure2 Homoploid and allopolyploid hybridization.jpg|thumb|Figure 2. Shematical representation of homoploid and allopolyploid hybrid speciation.]] ===Reproductive isolation against parent species=== To successfully establish as a hybrid species, reproductive isolation against both parent species is required [1,26,39]. This reproductive isolation can arise from either intrinsic postzygotic incompatibilities frequently causing inviability or sterility, or from extrinsic ecological incompatibilities where back crosses have reduced fitness [22]. Work on ''Helianthus'' sunflowers has revealed that pre-existing structural differences [35,40], in combination with hybridization induced structural differences [35] can cause reproductive isolation against the parent species. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in the reproductively isolated Italian sparrow [28]. Ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive traits [41], or through novel combinations of ecological traits from the parent species [42]. Differences in habitat use [41] or in phenology [43] will result in some degree of reproductive isolation against parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important ecological barrier [44-47]. Premating isolation generated from assortative mating between hybrids has been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [48]. A similar pattern was found in Galapagos finches where a specific hybrid beak shape and song are thought to have been important [8], and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species [12]. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [49]. Hence, under some conditions mate choice could form important reproductive barriers to gene flow. ===Hybrid genomes and genome stabilization=== Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve indepently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both these types of hybridization derived genomes as hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behavior and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [50]. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization» (Fig. 3). Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that recombination is suppressed near genes conferring reproductive isolation [51]. The strength of the supression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [51]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes [52], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [33]. In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations [53], whereas in hybrid ''Xiphophorus'' swordtail genomes [54] genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca 2000 generations after hybridization [55], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [56]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against intrinsic incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [20,57,58]; (Fig.3). An insecticide resistance region was retained following a hybridization event in the mosquito ''A. coluzzi'' [20], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in ''Mimulus'' plants [59], in ''Mus domesticus'' house mice [60], in humans [61] and in ''Xiphophorus'' swordtail fish [31]. In addition to recombination rate, the coupling to incompatible loci may be important for the likelihood of retention of introgressed material [57]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. Schematical representation of the process of hybrid genome stabilization.]] Genome-wide incompatibilities have been identified in swordtail fish [62], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids [63] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [32,64], fungus [65] and cyto-nuclear incompatibilities in ''Mimulus'' plants [66]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [32,63,67] and genes involved in mutagenesis and cancer related pathways [63] may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations [31,54,57]. Schumer and Brandvain found that hybridization-derived regions on average are less constrained than the rest of the genome [54]. During the process of hybrid genome stabilization minor parent genome content overrepresented in high recombination areas, both in swordtail fish and in humans [31]. In Italian sparrows, incompatible combinations have been purged through selective retention of ancestral sites [56]. The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [68-70], to activate transposable elements [71-73], and to induce chromosomal rearrangements [74,75]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [76,77]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana'' [78]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [79]. Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization [80]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [81,82]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [82,83]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration functional genes on a single chromosome and suggest that the reduction process partly is constrained [83]. A related allopolyploid specific phenomenon is sub genome dominance. For example, in the octoploid ''Fragaria'' strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homoeologous chromosomes are biased in favor of this subgenome, as compared with the other subgenomes [84]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [84]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissivley relative to the other subgenomes when brought together in the allopolyploid genome ([82] and [85]). Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [85]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [86,87]. Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [88]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [89], potentially buffering against a transcriptomic shock. ===In what taxa is hybridization common?=== While there is evidence for hybridization in an increasing number of taxa, sampling is not evenly distributed, and few general conclusions about the relative prevalence of hybridization can be drawn. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [90]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [91]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [92,93], and may hence enable hybridization between phylogenetically more distant taxa. Empirical evidence for Haldane’s rule [94] stating that when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex” supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [95]. These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [96]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see [97] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [98]. This pattern may reflect the lower effective population sizes and higher suceptibility to drift on the sex chromosomes [99], the elevated frequency of loci involved in reproductive isolation [100] and/or the heightened conflict on sex chromosomes [101]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [32] is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, autonomous selfing may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer [102]. Paradoxically, the ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [103]. In fungi, hybrids can be generated by asexual fusion of cells or hyphae [104] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [104]. Fungal hybridization may also result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species [105]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [106], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid genome formation. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity (primary hybridization) or between divergent taxa that come into secondary contact (secondary hybridization). Secondary hybridization is expected to have a greater potential to contribute beneficial alleles or generate novelty than primary hybridization because more divergent alleles are combined in secondary hybridization and are thus more likely to have a large fitness effect or to generate transgressive phenotypes [107]. The proportion of the genome that is inherited from a minority parent varies strongly among and within species. After the initial ploidization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [108]. Relatively equal parental contributions are also found in some homoploid hybrid species [36]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [31,32]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance [20] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly ''Heliconius numata'' [109]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [110]. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries [18,111,112], and examples include e.g. genes involved in olfaction that are introgressed across a mouse ''M. musculus'' and ''M. domesticus'' hybrid zone [113]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. [114]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occassional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enable adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybridization is frequent, the advantage of novel adaptive trait combinations often override the negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybridization is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [33,54]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does minority parent ancestry typically remain primarily in high recombination tracts c.f. [31] or are there generally stable solutions with high contributions from both parent species across the genome c.f. [32]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. [79,108]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana [80]? Hybrid genomes, including that of many individuals of our own species [55] are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ---- ==Box: Detecting and studying hybridization with genomic tools== Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE [116], ADMIXTURE [117] or fineSTRUCTURE [118]. These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. This method can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [119]. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a the gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests [120-122] or f-statistics [123,124]. Modified versions of these tests can be used to infer introgressed genomic regions [125], the direction of gene flow [126,127] or the amount of gene flow (Reich et al. 2009). These methods can also be used to infer the relative timing of introgression with the length of the introgressed tracts [9]. For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited [128-130]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that incomplete lineage sorting and hybridization may also help [131,132]. Methods based on linkage disequilibrium decay can be used to date recent admixture events as over time ancestry tracts are continuously broken down by recombination [129,133-136]. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [137]. Demographic modeling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [138,139] or with summary statistics in an Approximate Bayesian Computation framework [140]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [141]. ---- ==Glossary== Ancestry block/introgression tracts: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts form different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: intrinsic postmating barriers. These include both mechanical and other incompatibilities preventing egg fertilization, and hybrid inviability and/or sterility arising from incompatible combinations of genes, whereas extrinsic incompatibilities arise when trait combinations lead to reduced ecological fitness in the hybrid offspring. Pre-mating barriers: Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can occur classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. Recombination rate: Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinatorial hybrid speciation: the process by which a hybrid taxon develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 4y8t72hhp4vx3ucf63qrtj3sfdluzza 7465 7357 2019-03-26T06:22:52Z T Shafee 80 /* Wikipedia links */ ce wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Hybridization is the process where genetically closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is an important source of novel variation. Although most hybrids are sterile or less fit than their parents, some may be survive and reproduce and enable the transfer of adaptive variants across the species boundary, or even result in the formation of novel lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number. Homoploid hybrids can sort the intrinsic barriers that isolate the parent species from each other so that a subset of these isolate the hybrid species against each parent species, or gain pre-mating extrinsic isolation from ecological differences. Hybrid species may face problems arising from incompatible combinations of genes derived from different parent species. During the process of genome stabilization selection for compatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. ==Background== Genetic exchange between species can impede biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed hybridization as maladaptive sexual preferences [2] which resulted in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary force in animals [1,6,7]. Hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species [1]. Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches [8], African ''Haplochromis'' cichlid fishes [9], ''Heliconius'' butterflies [10-12] and Hawaiian ''Madiinae'' tarweeds and silverswords [13]. Here we review the evolutionary outcomes of hybridization and the properties of genomes of hybrid species. ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If hybrids are not viable or sterile, hybridization will not affect the parent species, except perhaps for a reduction in their reproductive success [14,15]. In contrast, if the fitness of hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [16,17]; Fig. 1). If the fitness of hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [18]. Hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct in spite of occassional gene flow [19,20]. In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [21,22]. Below we describe the evolutionary outcomes of hybridisation that result in hybrid genomes. [[File:Figure1 Potential evolutionary outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental specis can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from the mosquito ''Anopheles gambiae'' to ''A. coluzzii'' [20] and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta'' [23] and other ''Heliconius'' species [19]. In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from ''A. lyrata'' [24]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [25]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., a hybrid species [1,21]. A hybrid species has an admixed genome and forms stable genetically distinct populations [21]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion of a hybrid species [26], but see [27]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied homoploid hybrid species e.g. the butterfly ''Heliconius heurippa'' [10-12], the Italian sparrow ''Passer italiae'' [28], and three ''Helianthus'' sunflower species [29] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [26]. Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (introgressive speciation, c.f. [30]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinatorial hybrid speciation, [21]). A recombinatorial hybrid taxon typically also has a substantial proportion of the genome derived from the minority parent, although variation exist both between taxa and within lineages of hybrid taxa, see e.g. [31,32]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [27,29,33-37]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in increased ploidy compared to their parental taxa (Fig. 2). This form of hybrid speciation is more common in plants than in animals [38]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [38], but reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. [[File:Figure2 Homoploid and allopolyploid hybridization.jpg|thumb|Figure 2. Shematical representation of homoploid and allopolyploid hybrid speciation.]] ===Reproductive isolation against parent species=== To successfully establish as a hybrid species, reproductive isolation against both parent species is required [1,26,39]. This reproductive isolation can arise from either intrinsic postzygotic incompatibilities frequently causing inviability or sterility, or from extrinsic ecological incompatibilities where back crosses have reduced fitness [22]. Work on ''Helianthus'' sunflowers has revealed that pre-existing structural differences [35,40], in combination with hybridization induced structural differences [35] can cause reproductive isolation against the parent species. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in the reproductively isolated Italian sparrow [28]. Ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive traits [41], or through novel combinations of ecological traits from the parent species [42]. Differences in habitat use [41] or in phenology [43] will result in some degree of reproductive isolation against parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important ecological barrier [44-47]. Premating isolation generated from assortative mating between hybrids has been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [48]. A similar pattern was found in Galapagos finches where a specific hybrid beak shape and song are thought to have been important [8], and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species [12]. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [49]. Hence, under some conditions mate choice could form important reproductive barriers to gene flow. ===Hybrid genomes and genome stabilization=== Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve indepently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both these types of hybridization derived genomes as hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behavior and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [50]. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization» (Fig. 3). Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that recombination is suppressed near genes conferring reproductive isolation [51]. The strength of the supression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [51]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes [52], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [33]. In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations [53], whereas in hybrid ''Xiphophorus'' swordtail genomes [54] genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca 2000 generations after hybridization [55], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [56]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against intrinsic incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [20,57,58]; (Fig.3). An insecticide resistance region was retained following a hybridization event in the mosquito ''A. coluzzi'' [20], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in ''Mimulus'' plants [59], in ''Mus domesticus'' house mice [60], in humans [61] and in ''Xiphophorus'' swordtail fish [31]. In addition to recombination rate, the coupling to incompatible loci may be important for the likelihood of retention of introgressed material [57]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. Schematical representation of the process of hybrid genome stabilization.]] Genome-wide incompatibilities have been identified in swordtail fish [62], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids [63] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [32,64], fungus [65] and cyto-nuclear incompatibilities in ''Mimulus'' plants [66]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [32,63,67] and genes involved in mutagenesis and cancer related pathways [63] may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations [31,54,57]. Schumer and Brandvain found that hybridization-derived regions on average are less constrained than the rest of the genome [54]. During the process of hybrid genome stabilization minor parent genome content overrepresented in high recombination areas, both in swordtail fish and in humans [31]. In Italian sparrows, incompatible combinations have been purged through selective retention of ancestral sites [56]. The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [68-70], to activate transposable elements [71-73], and to induce chromosomal rearrangements [74,75]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [76,77]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana'' [78]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [79]. Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization [80]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [81,82]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [82,83]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration functional genes on a single chromosome and suggest that the reduction process partly is constrained [83]. A related allopolyploid specific phenomenon is sub genome dominance. For example, in the octoploid ''Fragaria'' strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homoeologous chromosomes are biased in favor of this subgenome, as compared with the other subgenomes [84]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [84]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissivley relative to the other subgenomes when brought together in the allopolyploid genome ([82] and [85]). Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [85]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [86,87]. Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [88]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [89], potentially buffering against a transcriptomic shock. ===In what taxa is hybridization common?=== While there is evidence for hybridization in an increasing number of taxa, sampling is not evenly distributed, and few general conclusions about the relative prevalence of hybridization can be drawn. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [90]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [91]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [92,93], and may hence enable hybridization between phylogenetically more distant taxa. Empirical evidence for Haldane’s rule [94] stating that when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex” supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [95]. These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [96]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see [97] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [98]. This pattern may reflect the lower effective population sizes and higher suceptibility to drift on the sex chromosomes [99], the elevated frequency of loci involved in reproductive isolation [100] and/or the heightened conflict on sex chromosomes [101]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [32] is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, autonomous selfing may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer [102]. Paradoxically, the ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [103]. In fungi, hybrids can be generated by asexual fusion of cells or hyphae [104] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [104]. Fungal hybridization may also result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species [105]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [106], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid genome formation. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity (primary hybridization) or between divergent taxa that come into secondary contact (secondary hybridization). Secondary hybridization is expected to have a greater potential to contribute beneficial alleles or generate novelty than primary hybridization because more divergent alleles are combined in secondary hybridization and are thus more likely to have a large fitness effect or to generate transgressive phenotypes [107]. The proportion of the genome that is inherited from a minority parent varies strongly among and within species. After the initial ploidization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [108]. Relatively equal parental contributions are also found in some homoploid hybrid species [36]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [31,32]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance [20] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly ''Heliconius numata'' [109]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [110]. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries [18,111,112], and examples include e.g. genes involved in olfaction that are introgressed across a mouse ''M. musculus'' and ''M. domesticus'' hybrid zone [113]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. [114]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occassional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enable adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybridization is frequent, the advantage of novel adaptive trait combinations often override the negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybridization is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [33,54]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does minority parent ancestry typically remain primarily in high recombination tracts c.f. [31] or are there generally stable solutions with high contributions from both parent species across the genome c.f. [32]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. [79,108]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana [80]? Hybrid genomes, including that of many individuals of our own species [55] are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ---- ==Box: Detecting and studying hybridization with genomic tools== Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE [116], ADMIXTURE [117] or fineSTRUCTURE [118]. These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. This method can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [119]. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a the gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests [120-122] or f-statistics [123,124]. Modified versions of these tests can be used to infer introgressed genomic regions [125], the direction of gene flow [126,127] or the amount of gene flow (Reich et al. 2009). These methods can also be used to infer the relative timing of introgression with the length of the introgressed tracts [9]. For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited [128-130]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that incomplete lineage sorting and hybridization may also help [131,132]. Methods based on linkage disequilibrium decay can be used to date recent admixture events as over time ancestry tracts are continuously broken down by recombination [129,133-136]. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [137]. Demographic modeling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [138,139] or with summary statistics in an Approximate Bayesian Computation framework [140]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [141]. ---- ==Glossary== Ancestry block/introgression tracts: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts form different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: intrinsic postmating barriers. These include both mechanical and other incompatibilities preventing egg fertilization, and hybrid inviability and/or sterility arising from incompatible combinations of genes, whereas extrinsic incompatibilities arise when trait combinations lead to reduced ecological fitness in the hybrid offspring. Pre-mating barriers: Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can occur classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. Recombination rate: Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinatorial hybrid speciation: the process by which a hybrid taxon develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 mu1ziyg8vr4oai1twpu82qn6za51qk1 7466 7465 2019-03-26T06:23:49Z T Shafee 80 /* References */ ce wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Hybridization is the process where genetically closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is an important source of novel variation. Although most hybrids are sterile or less fit than their parents, some may be survive and reproduce and enable the transfer of adaptive variants across the species boundary, or even result in the formation of novel lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number. Homoploid hybrids can sort the intrinsic barriers that isolate the parent species from each other so that a subset of these isolate the hybrid species against each parent species, or gain pre-mating extrinsic isolation from ecological differences. Hybrid species may face problems arising from incompatible combinations of genes derived from different parent species. During the process of genome stabilization selection for compatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. ==Background== Genetic exchange between species can impede biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed hybridization as maladaptive sexual preferences [2] which resulted in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary force in animals [1,6,7]. Hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species [1]. Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches [8], African ''Haplochromis'' cichlid fishes [9], ''Heliconius'' butterflies [10-12] and Hawaiian ''Madiinae'' tarweeds and silverswords [13]. Here we review the evolutionary outcomes of hybridization and the properties of genomes of hybrid species. ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If hybrids are not viable or sterile, hybridization will not affect the parent species, except perhaps for a reduction in their reproductive success [14,15]. In contrast, if the fitness of hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [16,17]; Fig. 1). If the fitness of hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [18]. Hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct in spite of occassional gene flow [19,20]. In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [21,22]. Below we describe the evolutionary outcomes of hybridisation that result in hybrid genomes. [[File:Figure1 Potential evolutionary outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental specis can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from the mosquito ''Anopheles gambiae'' to ''A. coluzzii'' [20] and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta'' [23] and other ''Heliconius'' species [19]. In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from ''A. lyrata'' [24]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [25]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., a hybrid species [1,21]. A hybrid species has an admixed genome and forms stable genetically distinct populations [21]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion of a hybrid species [26], but see [27]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied homoploid hybrid species e.g. the butterfly ''Heliconius heurippa'' [10-12], the Italian sparrow ''Passer italiae'' [28], and three ''Helianthus'' sunflower species [29] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [26]. Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (introgressive speciation, c.f. [30]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinatorial hybrid speciation, [21]). A recombinatorial hybrid taxon typically also has a substantial proportion of the genome derived from the minority parent, although variation exist both between taxa and within lineages of hybrid taxa, see e.g. [31,32]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [27,29,33-37]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in increased ploidy compared to their parental taxa (Fig. 2). This form of hybrid speciation is more common in plants than in animals [38]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [38], but reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. [[File:Figure2 Homoploid and allopolyploid hybridization.jpg|thumb|Figure 2. Shematical representation of homoploid and allopolyploid hybrid speciation.]] ===Reproductive isolation against parent species=== To successfully establish as a hybrid species, reproductive isolation against both parent species is required [1,26,39]. This reproductive isolation can arise from either intrinsic postzygotic incompatibilities frequently causing inviability or sterility, or from extrinsic ecological incompatibilities where back crosses have reduced fitness [22]. Work on ''Helianthus'' sunflowers has revealed that pre-existing structural differences [35,40], in combination with hybridization induced structural differences [35] can cause reproductive isolation against the parent species. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in the reproductively isolated Italian sparrow [28]. Ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive traits [41], or through novel combinations of ecological traits from the parent species [42]. Differences in habitat use [41] or in phenology [43] will result in some degree of reproductive isolation against parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important ecological barrier [44-47]. Premating isolation generated from assortative mating between hybrids has been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [48]. A similar pattern was found in Galapagos finches where a specific hybrid beak shape and song are thought to have been important [8], and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species [12]. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [49]. Hence, under some conditions mate choice could form important reproductive barriers to gene flow. ===Hybrid genomes and genome stabilization=== Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve indepently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both these types of hybridization derived genomes as hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behavior and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [50]. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization» (Fig. 3). Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that recombination is suppressed near genes conferring reproductive isolation [51]. The strength of the supression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [51]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes [52], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [33]. In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations [53], whereas in hybrid ''Xiphophorus'' swordtail genomes [54] genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca 2000 generations after hybridization [55], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [56]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against intrinsic incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [20,57,58]; (Fig.3). An insecticide resistance region was retained following a hybridization event in the mosquito ''A. coluzzi'' [20], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in ''Mimulus'' plants [59], in ''Mus domesticus'' house mice [60], in humans [61] and in ''Xiphophorus'' swordtail fish [31]. In addition to recombination rate, the coupling to incompatible loci may be important for the likelihood of retention of introgressed material [57]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. Schematical representation of the process of hybrid genome stabilization.]] Genome-wide incompatibilities have been identified in swordtail fish [62], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids [63] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [32,64], fungus [65] and cyto-nuclear incompatibilities in ''Mimulus'' plants [66]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [32,63,67] and genes involved in mutagenesis and cancer related pathways [63] may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations [31,54,57]. Schumer and Brandvain found that hybridization-derived regions on average are less constrained than the rest of the genome [54]. During the process of hybrid genome stabilization minor parent genome content overrepresented in high recombination areas, both in swordtail fish and in humans [31]. In Italian sparrows, incompatible combinations have been purged through selective retention of ancestral sites [56]. The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [68-70], to activate transposable elements [71-73], and to induce chromosomal rearrangements [74,75]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [76,77]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana'' [78]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [79]. Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization [80]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [81,82]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [82,83]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration functional genes on a single chromosome and suggest that the reduction process partly is constrained [83]. A related allopolyploid specific phenomenon is sub genome dominance. For example, in the octoploid ''Fragaria'' strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homoeologous chromosomes are biased in favor of this subgenome, as compared with the other subgenomes [84]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [84]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissivley relative to the other subgenomes when brought together in the allopolyploid genome ([82] and [85]). Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [85]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [86,87]. Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [88]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [89], potentially buffering against a transcriptomic shock. ===In what taxa is hybridization common?=== While there is evidence for hybridization in an increasing number of taxa, sampling is not evenly distributed, and few general conclusions about the relative prevalence of hybridization can be drawn. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [90]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [91]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [92,93], and may hence enable hybridization between phylogenetically more distant taxa. Empirical evidence for Haldane’s rule [94] stating that when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex” supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [95]. These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [96]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see [97] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [98]. This pattern may reflect the lower effective population sizes and higher suceptibility to drift on the sex chromosomes [99], the elevated frequency of loci involved in reproductive isolation [100] and/or the heightened conflict on sex chromosomes [101]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [32] is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, autonomous selfing may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer [102]. Paradoxically, the ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [103]. In fungi, hybrids can be generated by asexual fusion of cells or hyphae [104] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [104]. Fungal hybridization may also result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species [105]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [106], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid genome formation. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity (primary hybridization) or between divergent taxa that come into secondary contact (secondary hybridization). Secondary hybridization is expected to have a greater potential to contribute beneficial alleles or generate novelty than primary hybridization because more divergent alleles are combined in secondary hybridization and are thus more likely to have a large fitness effect or to generate transgressive phenotypes [107]. The proportion of the genome that is inherited from a minority parent varies strongly among and within species. After the initial ploidization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [108]. Relatively equal parental contributions are also found in some homoploid hybrid species [36]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [31,32]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance [20] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly ''Heliconius numata'' [109]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [110]. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries [18,111,112], and examples include e.g. genes involved in olfaction that are introgressed across a mouse ''M. musculus'' and ''M. domesticus'' hybrid zone [113]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. [114]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occassional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enable adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybridization is frequent, the advantage of novel adaptive trait combinations often override the negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybridization is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [33,54]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does minority parent ancestry typically remain primarily in high recombination tracts c.f. [31] or are there generally stable solutions with high contributions from both parent species across the genome c.f. [32]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. [79,108]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana [80]? Hybrid genomes, including that of many individuals of our own species [55] are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ---- ==Box: Detecting and studying hybridization with genomic tools== Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE [116], ADMIXTURE [117] or fineSTRUCTURE [118]. These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. This method can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [119]. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a the gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests [120-122] or f-statistics [123,124]. Modified versions of these tests can be used to infer introgressed genomic regions [125], the direction of gene flow [126,127] or the amount of gene flow (Reich et al. 2009). These methods can also be used to infer the relative timing of introgression with the length of the introgressed tracts [9]. For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited [128-130]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that incomplete lineage sorting and hybridization may also help [131,132]. Methods based on linkage disequilibrium decay can be used to date recent admixture events as over time ancestry tracts are continuously broken down by recombination [129,133-136]. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [137]. Demographic modeling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [138,139] or with summary statistics in an Approximate Bayesian Computation framework [140]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [141]. ---- ==Glossary== Ancestry block/introgression tracts: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts form different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: intrinsic postmating barriers. These include both mechanical and other incompatibilities preventing egg fertilization, and hybrid inviability and/or sterility arising from incompatible combinations of genes, whereas extrinsic incompatibilities arise when trait combinations lead to reduced ecological fitness in the hybrid offspring. Pre-mating barriers: Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can occur classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. Recombination rate: Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinatorial hybrid speciation: the process by which a hybrid taxon develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 rq3oehtgaoi4hiq4zw5h5izu10qkkjp 7467 7466 2019-03-26T06:24:47Z T Shafee 80 /* References */ ce wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Hybridization is the process where genetically closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is an important source of novel variation. Although most hybrids are sterile or less fit than their parents, some may be survive and reproduce and enable the transfer of adaptive variants across the species boundary, or even result in the formation of novel lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number. Homoploid hybrids can sort the intrinsic barriers that isolate the parent species from each other so that a subset of these isolate the hybrid species against each parent species, or gain pre-mating extrinsic isolation from ecological differences. Hybrid species may face problems arising from incompatible combinations of genes derived from different parent species. During the process of genome stabilization selection for compatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. ==Background== Genetic exchange between species can impede biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed hybridization as maladaptive sexual preferences [2] which resulted in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary force in animals [1,6,7]. Hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species [1]. Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches [8], African ''Haplochromis'' cichlid fishes [9], ''Heliconius'' butterflies [10-12] and Hawaiian ''Madiinae'' tarweeds and silverswords [13]. Here we review the evolutionary outcomes of hybridization and the properties of genomes of hybrid species. ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If hybrids are not viable or sterile, hybridization will not affect the parent species, except perhaps for a reduction in their reproductive success [14,15]. In contrast, if the fitness of hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [16,17]; Fig. 1). If the fitness of hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [18]. Hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct in spite of occassional gene flow [19,20]. In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [21,22]. Below we describe the evolutionary outcomes of hybridisation that result in hybrid genomes. [[File:Figure1 Potential evolutionary outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental specis can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from the mosquito ''Anopheles gambiae'' to ''A. coluzzii'' [20] and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta'' [23] and other ''Heliconius'' species [19]. In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from ''A. lyrata'' [24]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [25]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., a hybrid species [1,21]. A hybrid species has an admixed genome and forms stable genetically distinct populations [21]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion of a hybrid species [26], but see [27]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied homoploid hybrid species e.g. the butterfly ''Heliconius heurippa'' [10-12], the Italian sparrow ''Passer italiae'' [28], and three ''Helianthus'' sunflower species [29] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [26]. Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (introgressive speciation, c.f. [30]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinatorial hybrid speciation, [21]). A recombinatorial hybrid taxon typically also has a substantial proportion of the genome derived from the minority parent, although variation exist both between taxa and within lineages of hybrid taxa, see e.g. [31,32]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [27,29,33-37]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in increased ploidy compared to their parental taxa (Fig. 2). This form of hybrid speciation is more common in plants than in animals [38]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [38], but reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. [[File:Figure2 Homoploid and allopolyploid hybridization.jpg|thumb|Figure 2. Shematical representation of homoploid and allopolyploid hybrid speciation.]] ===Reproductive isolation against parent species=== To successfully establish as a hybrid species, reproductive isolation against both parent species is required [1,26,39]. This reproductive isolation can arise from either intrinsic postzygotic incompatibilities frequently causing inviability or sterility, or from extrinsic ecological incompatibilities where back crosses have reduced fitness [22]. Work on ''Helianthus'' sunflowers has revealed that pre-existing structural differences [35,40], in combination with hybridization induced structural differences [35] can cause reproductive isolation against the parent species. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in the reproductively isolated Italian sparrow [28]. Ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive traits [41], or through novel combinations of ecological traits from the parent species [42]. Differences in habitat use [41] or in phenology [43] will result in some degree of reproductive isolation against parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important ecological barrier [44-47]. Premating isolation generated from assortative mating between hybrids has been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [48]. A similar pattern was found in Galapagos finches where a specific hybrid beak shape and song are thought to have been important [8], and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species [12]. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [49]. Hence, under some conditions mate choice could form important reproductive barriers to gene flow. ===Hybrid genomes and genome stabilization=== Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve indepently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both these types of hybridization derived genomes as hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behavior and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [50]. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization» (Fig. 3). Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that recombination is suppressed near genes conferring reproductive isolation [51]. The strength of the supression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [51]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes [52], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [33]. In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations [53], whereas in hybrid ''Xiphophorus'' swordtail genomes [54] genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca 2000 generations after hybridization [55], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [56]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against intrinsic incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [20,57,58]; (Fig.3). An insecticide resistance region was retained following a hybridization event in the mosquito ''A. coluzzi'' [20], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in ''Mimulus'' plants [59], in ''Mus domesticus'' house mice [60], in humans [61] and in ''Xiphophorus'' swordtail fish [31]. In addition to recombination rate, the coupling to incompatible loci may be important for the likelihood of retention of introgressed material [57]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. Schematical representation of the process of hybrid genome stabilization.]] Genome-wide incompatibilities have been identified in swordtail fish [62], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids [63] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [32,64], fungus [65] and cyto-nuclear incompatibilities in ''Mimulus'' plants [66]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [32,63,67] and genes involved in mutagenesis and cancer related pathways [63] may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations [31,54,57]. Schumer and Brandvain found that hybridization-derived regions on average are less constrained than the rest of the genome [54]. During the process of hybrid genome stabilization minor parent genome content overrepresented in high recombination areas, both in swordtail fish and in humans [31]. In Italian sparrows, incompatible combinations have been purged through selective retention of ancestral sites [56]. The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [68-70], to activate transposable elements [71-73], and to induce chromosomal rearrangements [74,75]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [76,77]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana'' [78]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [79]. Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization [80]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [81,82]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [82,83]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration functional genes on a single chromosome and suggest that the reduction process partly is constrained [83]. A related allopolyploid specific phenomenon is sub genome dominance. For example, in the octoploid ''Fragaria'' strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homoeologous chromosomes are biased in favor of this subgenome, as compared with the other subgenomes [84]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [84]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissivley relative to the other subgenomes when brought together in the allopolyploid genome ([82] and [85]). Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [85]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [86,87]. Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [88]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [89], potentially buffering against a transcriptomic shock. ===In what taxa is hybridization common?=== While there is evidence for hybridization in an increasing number of taxa, sampling is not evenly distributed, and few general conclusions about the relative prevalence of hybridization can be drawn. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [90]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [91]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [92,93], and may hence enable hybridization between phylogenetically more distant taxa. Empirical evidence for Haldane’s rule [94] stating that when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex” supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [95]. These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [96]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see [97] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [98]. This pattern may reflect the lower effective population sizes and higher suceptibility to drift on the sex chromosomes [99], the elevated frequency of loci involved in reproductive isolation [100] and/or the heightened conflict on sex chromosomes [101]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [32] is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, autonomous selfing may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer [102]. Paradoxically, the ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [103]. In fungi, hybrids can be generated by asexual fusion of cells or hyphae [104] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [104]. Fungal hybridization may also result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species [105]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [106], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid genome formation. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity (primary hybridization) or between divergent taxa that come into secondary contact (secondary hybridization). Secondary hybridization is expected to have a greater potential to contribute beneficial alleles or generate novelty than primary hybridization because more divergent alleles are combined in secondary hybridization and are thus more likely to have a large fitness effect or to generate transgressive phenotypes [107]. The proportion of the genome that is inherited from a minority parent varies strongly among and within species. After the initial ploidization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [108]. Relatively equal parental contributions are also found in some homoploid hybrid species [36]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [31,32]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance [20] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly ''Heliconius numata'' [109]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [110]. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries [18,111,112], and examples include e.g. genes involved in olfaction that are introgressed across a mouse ''M. musculus'' and ''M. domesticus'' hybrid zone [113]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. [114]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occassional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enable adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybridization is frequent, the advantage of novel adaptive trait combinations often override the negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybridization is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [33,54]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does minority parent ancestry typically remain primarily in high recombination tracts c.f. [31] or are there generally stable solutions with high contributions from both parent species across the genome c.f. [32]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. [79,108]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana [80]? Hybrid genomes, including that of many individuals of our own species [55] are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ---- ==Box: Detecting and studying hybridization with genomic tools== Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE [116], ADMIXTURE [117] or fineSTRUCTURE [118]. These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. This method can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [119]. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a the gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests [120-122] or f-statistics [123,124]. Modified versions of these tests can be used to infer introgressed genomic regions [125], the direction of gene flow [126,127] or the amount of gene flow (Reich et al. 2009). These methods can also be used to infer the relative timing of introgression with the length of the introgressed tracts [9]. For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited [128-130]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that incomplete lineage sorting and hybridization may also help [131,132]. Methods based on linkage disequilibrium decay can be used to date recent admixture events as over time ancestry tracts are continuously broken down by recombination [129,133-136]. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [137]. Demographic modeling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [138,139] or with summary statistics in an Approximate Bayesian Computation framework [140]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [141]. ---- ==Glossary== Ancestry block/introgression tracts: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts form different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: intrinsic postmating barriers. These include both mechanical and other incompatibilities preventing egg fertilization, and hybrid inviability and/or sterility arising from incompatible combinations of genes, whereas extrinsic incompatibilities arise when trait combinations lead to reduced ecological fitness in the hybrid offspring. Pre-mating barriers: Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can occur classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. Recombination rate: Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinatorial hybrid speciation: the process by which a hybrid taxon develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 ofbrlx65xsbw6wpb6c41u0jphpyrnaf 7469 7467 2019-03-26T06:29:21Z T Shafee 80 image as svg wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Hybridization is the process where genetically closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is an important source of novel variation. Although most hybrids are sterile or less fit than their parents, some may be survive and reproduce and enable the transfer of adaptive variants across the species boundary, or even result in the formation of novel lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number. Homoploid hybrids can sort the intrinsic barriers that isolate the parent species from each other so that a subset of these isolate the hybrid species against each parent species, or gain pre-mating extrinsic isolation from ecological differences. Hybrid species may face problems arising from incompatible combinations of genes derived from different parent species. During the process of genome stabilization selection for compatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. ==Background== Genetic exchange between species can impede biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed hybridization as maladaptive sexual preferences [2] which resulted in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary force in animals [1,6,7]. Hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species [1]. Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches [8], African ''Haplochromis'' cichlid fishes [9], ''Heliconius'' butterflies [10-12] and Hawaiian ''Madiinae'' tarweeds and silverswords [13]. Here we review the evolutionary outcomes of hybridization and the properties of genomes of hybrid species. ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If hybrids are not viable or sterile, hybridization will not affect the parent species, except perhaps for a reduction in their reproductive success [14,15]. In contrast, if the fitness of hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [16,17]; Fig. 1). If the fitness of hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [18]. Hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct in spite of occassional gene flow [19,20]. In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [21,22]. Below we describe the evolutionary outcomes of hybridisation that result in hybrid genomes. [[File:Figure1 Potential evolutionary outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental specis can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from the mosquito ''Anopheles gambiae'' to ''A. coluzzii'' [20] and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta'' [23] and other ''Heliconius'' species [19]. In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from ''A. lyrata'' [24]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [25]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., a hybrid species [1,21]. A hybrid species has an admixed genome and forms stable genetically distinct populations [21]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion of a hybrid species [26], but see [27]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied homoploid hybrid species e.g. the butterfly ''Heliconius heurippa'' [10-12], the Italian sparrow ''Passer italiae'' [28], and three ''Helianthus'' sunflower species [29] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [26]. Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (introgressive speciation, c.f. [30]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinatorial hybrid speciation, [21]). A recombinatorial hybrid taxon typically also has a substantial proportion of the genome derived from the minority parent, although variation exist both between taxa and within lineages of hybrid taxa, see e.g. [31,32]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [27,29,33-37]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in increased ploidy compared to their parental taxa (Fig. 2). This form of hybrid speciation is more common in plants than in animals [38]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [38], but reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. [[File:Figure2 Homoploid and allopolyploid hybridization.svg|thumb|Figure 2. Shematical representation of homoploid and allopolyploid hybrid speciation.]] ===Reproductive isolation against parent species=== To successfully establish as a hybrid species, reproductive isolation against both parent species is required [1,26,39]. This reproductive isolation can arise from either intrinsic postzygotic incompatibilities frequently causing inviability or sterility, or from extrinsic ecological incompatibilities where back crosses have reduced fitness [22]. Work on ''Helianthus'' sunflowers has revealed that pre-existing structural differences [35,40], in combination with hybridization induced structural differences [35] can cause reproductive isolation against the parent species. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in the reproductively isolated Italian sparrow [28]. Ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive traits [41], or through novel combinations of ecological traits from the parent species [42]. Differences in habitat use [41] or in phenology [43] will result in some degree of reproductive isolation against parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important ecological barrier [44-47]. Premating isolation generated from assortative mating between hybrids has been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [48]. A similar pattern was found in Galapagos finches where a specific hybrid beak shape and song are thought to have been important [8], and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species [12]. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [49]. Hence, under some conditions mate choice could form important reproductive barriers to gene flow. ===Hybrid genomes and genome stabilization=== Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve indepently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both these types of hybridization derived genomes as hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behavior and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [50]. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization» (Fig. 3). Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that recombination is suppressed near genes conferring reproductive isolation [51]. The strength of the supression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [51]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes [52], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [33]. In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations [53], whereas in hybrid ''Xiphophorus'' swordtail genomes [54] genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca 2000 generations after hybridization [55], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [56]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against intrinsic incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [20,57,58]; (Fig.3). An insecticide resistance region was retained following a hybridization event in the mosquito ''A. coluzzi'' [20], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in ''Mimulus'' plants [59], in ''Mus domesticus'' house mice [60], in humans [61] and in ''Xiphophorus'' swordtail fish [31]. In addition to recombination rate, the coupling to incompatible loci may be important for the likelihood of retention of introgressed material [57]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. Schematical representation of the process of hybrid genome stabilization.]] Genome-wide incompatibilities have been identified in swordtail fish [62], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids [63] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [32,64], fungus [65] and cyto-nuclear incompatibilities in ''Mimulus'' plants [66]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [32,63,67] and genes involved in mutagenesis and cancer related pathways [63] may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations [31,54,57]. Schumer and Brandvain found that hybridization-derived regions on average are less constrained than the rest of the genome [54]. During the process of hybrid genome stabilization minor parent genome content overrepresented in high recombination areas, both in swordtail fish and in humans [31]. In Italian sparrows, incompatible combinations have been purged through selective retention of ancestral sites [56]. The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [68-70], to activate transposable elements [71-73], and to induce chromosomal rearrangements [74,75]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [76,77]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana'' [78]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [79]. Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization [80]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [81,82]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [82,83]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration functional genes on a single chromosome and suggest that the reduction process partly is constrained [83]. A related allopolyploid specific phenomenon is sub genome dominance. For example, in the octoploid ''Fragaria'' strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homoeologous chromosomes are biased in favor of this subgenome, as compared with the other subgenomes [84]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [84]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissivley relative to the other subgenomes when brought together in the allopolyploid genome ([82] and [85]). Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [85]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [86,87]. Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [88]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [89], potentially buffering against a transcriptomic shock. ===In what taxa is hybridization common?=== While there is evidence for hybridization in an increasing number of taxa, sampling is not evenly distributed, and few general conclusions about the relative prevalence of hybridization can be drawn. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [90]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [91]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [92,93], and may hence enable hybridization between phylogenetically more distant taxa. Empirical evidence for Haldane’s rule [94] stating that when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex” supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [95]. These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [96]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see [97] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [98]. This pattern may reflect the lower effective population sizes and higher suceptibility to drift on the sex chromosomes [99], the elevated frequency of loci involved in reproductive isolation [100] and/or the heightened conflict on sex chromosomes [101]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [32] is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, autonomous selfing may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer [102]. Paradoxically, the ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [103]. In fungi, hybrids can be generated by asexual fusion of cells or hyphae [104] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [104]. Fungal hybridization may also result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species [105]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [106], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid genome formation. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity (primary hybridization) or between divergent taxa that come into secondary contact (secondary hybridization). Secondary hybridization is expected to have a greater potential to contribute beneficial alleles or generate novelty than primary hybridization because more divergent alleles are combined in secondary hybridization and are thus more likely to have a large fitness effect or to generate transgressive phenotypes [107]. The proportion of the genome that is inherited from a minority parent varies strongly among and within species. After the initial ploidization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [108]. Relatively equal parental contributions are also found in some homoploid hybrid species [36]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [31,32]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance [20] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly ''Heliconius numata'' [109]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [110]. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries [18,111,112], and examples include e.g. genes involved in olfaction that are introgressed across a mouse ''M. musculus'' and ''M. domesticus'' hybrid zone [113]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. [114]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occassional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enable adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybridization is frequent, the advantage of novel adaptive trait combinations often override the negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybridization is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [33,54]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does minority parent ancestry typically remain primarily in high recombination tracts c.f. [31] or are there generally stable solutions with high contributions from both parent species across the genome c.f. [32]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. [79,108]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana [80]? Hybrid genomes, including that of many individuals of our own species [55] are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ---- ==Box: Detecting and studying hybridization with genomic tools== Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE [116], ADMIXTURE [117] or fineSTRUCTURE [118]. These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. This method can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [119]. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a the gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests [120-122] or f-statistics [123,124]. Modified versions of these tests can be used to infer introgressed genomic regions [125], the direction of gene flow [126,127] or the amount of gene flow (Reich et al. 2009). These methods can also be used to infer the relative timing of introgression with the length of the introgressed tracts [9]. For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited [128-130]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that incomplete lineage sorting and hybridization may also help [131,132]. Methods based on linkage disequilibrium decay can be used to date recent admixture events as over time ancestry tracts are continuously broken down by recombination [129,133-136]. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [137]. Demographic modeling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [138,139] or with summary statistics in an Approximate Bayesian Computation framework [140]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [141]. ---- ==Glossary== Ancestry block/introgression tracts: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts form different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: intrinsic postmating barriers. These include both mechanical and other incompatibilities preventing egg fertilization, and hybrid inviability and/or sterility arising from incompatible combinations of genes, whereas extrinsic incompatibilities arise when trait combinations lead to reduced ecological fitness in the hybrid offspring. Pre-mating barriers: Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can occur classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. Recombination rate: Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinatorial hybrid speciation: the process by which a hybrid taxon develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 ajdnjto4s214otwg0ajj77sf1mvt8q6 7571 7469 2019-04-15T14:36:27Z Eratosignis 140 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Hybridization is the process where genetically closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is an important source of novel variation. Although most hybrids are sterile or less fit than their parents, some may be survive and reproduce and enable the transfer of adaptive variants across the species boundary, or even result in the formation of novel lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number. Homoploid hybrids can sort the intrinsic barriers that isolate the parent species from each other so that a subset of these isolate the hybrid species against each parent species, or gain pre-mating extrinsic isolation from ecological differences. Hybrid species may face problems arising from incompatible combinations of genes derived from different parent species. During the process of genome stabilization selection for compatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. ==Background== Genetic exchange between species can impede biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed hybridization as maladaptive [2] which resulted in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary force in animals [1,6,7]. Hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species [1]. Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches [8], African ''Haplochromis'' cichlid fishes [9], ''Heliconius'' butterflies [10-12] and Hawaiian ''Madiinae'' tarweeds and silverswords [13]. Here we review the evolutionary outcomes of hybridization and the properties of genomes of hybrid species. ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If hybrids are not viable or sterile, hybridization will not affect the parent species, except perhaps for a reduction in their reproductive success [14,15]. In contrast, if the fitness of hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [16,17]; Fig. 1). If the fitness of hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [18]. Hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct in spite of occassional gene flow [19,20]. In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [21,22]. Below we describe the evolutionary outcomes of hybridisation that result in hybrid genomes. [[File:Figure1 Potential evolutionary outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental specis can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from the mosquito ''Anopheles gambiae'' to ''A. coluzzii'' [20] and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta'' [23] and other ''Heliconius'' species [19]. In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from ''A. lyrata'' [24]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [25]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., a hybrid species [1,21]. A hybrid species has an admixed genome and forms stable genetically distinct populations [21]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion of a hybrid species [26], but see [27]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied homoploid hybrid species e.g. the butterfly ''Heliconius heurippa'' [10-12], the Italian sparrow ''Passer italiae'' [28], and three ''Helianthus'' sunflower species [29] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [26]. Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (introgressive speciation, c.f. [30]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinatorial hybrid speciation, [21]). A recombinatorial hybrid taxon typically also has a substantial proportion of the genome derived from the minority parent, although variation exist both between taxa and within lineages of hybrid taxa, see e.g. [31,32]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [27,29,33-37]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in increased ploidy compared to their parental taxa (Fig. 2). This form of hybrid speciation is more common in plants than in animals [38]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [38], but reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. [[File:Figure2 Homoploid and allopolyploid hybridization.svg|thumb|Figure 2. Shematical representation of homoploid and allopolyploid hybrid speciation.]] ===Reproductive isolation against parent species=== To successfully establish as a hybrid species, reproductive isolation against both parent species is required [1,26,39]. This reproductive isolation can arise from either intrinsic postzygotic incompatibilities frequently causing inviability or sterility, or from extrinsic ecological incompatibilities where back crosses have reduced fitness [22]. Work on ''Helianthus'' sunflowers has revealed that pre-existing structural differences [35,40], in combination with hybridization induced structural differences [35] can cause reproductive isolation against the parent species. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in the reproductively isolated Italian sparrow [28]. Ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive traits [41], or through novel combinations of ecological traits from the parent species [42]. Differences in habitat use [41] or in phenology [43] will result in some degree of reproductive isolation against parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important ecological barrier [44-47]. Premating isolation generated from assortative mating between hybrids has been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [48]. A similar pattern was found in Galapagos finches where a specific hybrid beak shape and song are thought to have been important [8], and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species [12]. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [49]. Hence, under some conditions mate choice could form important reproductive barriers to gene flow. ===Hybrid genomes and genome stabilization=== Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve indepently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both these types of hybridization derived genomes as hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behavior and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [50]. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization» (Fig. 3). Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that recombination is suppressed near genes conferring reproductive isolation [51]. The strength of the supression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [51]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes [52], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [33]. In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations [53], whereas in hybrid ''Xiphophorus'' swordtail genomes [54] genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca 2000 generations after hybridization [55], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [56]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against intrinsic incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [20,57,58]; (Fig.3). An insecticide resistance region was retained following a hybridization event in the mosquito ''A. coluzzi'' [20], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in ''Mimulus'' plants [59], in ''Mus domesticus'' house mice [60], in humans [61] and in ''Xiphophorus'' swordtail fish [31]. In addition to recombination rate, the coupling to incompatible loci may be important for the likelihood of retention of introgressed material [57]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. Schematical representation of the process of hybrid genome stabilization.]] Genome-wide incompatibilities have been identified in swordtail fish [62], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids [63] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [32,64], fungus [65] and cyto-nuclear incompatibilities in ''Mimulus'' plants [66]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [32,63,67] and genes involved in mutagenesis and cancer related pathways [63] may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations [31,54,57]. Schumer and Brandvain found that hybridization-derived regions on average are less constrained than the rest of the genome [54]. During the process of hybrid genome stabilization minor parent genome content overrepresented in high recombination areas, both in swordtail fish and in humans [31]. In Italian sparrows, incompatible combinations have been purged through selective retention of ancestral sites [56]. The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [68-70], to activate transposable elements [71-73], and to induce chromosomal rearrangements [74,75]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [76,77]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana'' [78]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [79]. Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization [80]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [81,82]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [82,83]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration functional genes on a single chromosome and suggest that the reduction process partly is constrained [83]. A related allopolyploid specific phenomenon is sub genome dominance. For example, in the octoploid ''Fragaria'' strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homoeologous chromosomes are biased in favor of this subgenome, as compared with the other subgenomes [84]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [84]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissivley relative to the other subgenomes when brought together in the allopolyploid genome ([82] and [85]). Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [85]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [86,87]. Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [88]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [89], potentially buffering against a transcriptomic shock. ===In what taxa is hybridization common?=== While there is evidence for hybridization in an increasing number of taxa, sampling is not evenly distributed, and few general conclusions about the relative prevalence of hybridization can be drawn. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [90]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [91]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [92,93], and may hence enable hybridization between phylogenetically more distant taxa. Empirical evidence for Haldane’s rule [94] stating that when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex” supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [95]. These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [96]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see [97] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [98]. This pattern may reflect the lower effective population sizes and higher suceptibility to drift on the sex chromosomes [99], the elevated frequency of loci involved in reproductive isolation [100] and/or the heightened conflict on sex chromosomes [101]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [32] is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, autonomous selfing may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer [102]. Paradoxically, the ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [103]. In fungi, hybrids can be generated by asexual fusion of cells or hyphae [104] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [104]. Fungal hybridization may also result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species [105]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [106], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid genome formation. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity (primary hybridization) or between divergent taxa that come into secondary contact (secondary hybridization). Secondary hybridization is expected to have a greater potential to contribute beneficial alleles or generate novelty than primary hybridization because more divergent alleles are combined in secondary hybridization and are thus more likely to have a large fitness effect or to generate transgressive phenotypes [107]. The proportion of the genome that is inherited from a minority parent varies strongly among and within species. After the initial ploidization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [108]. Relatively equal parental contributions are also found in some homoploid hybrid species [36]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [31,32]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance [20] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly ''Heliconius numata'' [109]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [110]. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries [18,111,112], and examples include e.g. genes involved in olfaction that are introgressed across a mouse ''M. musculus'' and ''M. domesticus'' hybrid zone [113]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. [114]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occassional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enable adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybridization is frequent, the advantage of novel adaptive trait combinations often override the negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybridization is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [33,54]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does minority parent ancestry typically remain primarily in high recombination tracts c.f. [31] or are there generally stable solutions with high contributions from both parent species across the genome c.f. [32]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. [79,108]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana [80]? Hybrid genomes, including that of many individuals of our own species [55] are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ---- ==Box: Detecting and studying hybridization with genomic tools== Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE [116], ADMIXTURE [117] or fineSTRUCTURE [118]. These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. This method can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [119]. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a the gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests [120-122] or f-statistics [123,124]. Modified versions of these tests can be used to infer introgressed genomic regions [125], the direction of gene flow [126,127] or the amount of gene flow (Reich et al. 2009). These methods can also be used to infer the relative timing of introgression with the length of the introgressed tracts [9]. For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited [128-130]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that incomplete lineage sorting and hybridization may also help [131,132]. Methods based on linkage disequilibrium decay can be used to date recent admixture events as over time ancestry tracts are continuously broken down by recombination [129,133-136]. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [137]. Demographic modeling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [138,139] or with summary statistics in an Approximate Bayesian Computation framework [140]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [141]. ---- ==Glossary== Ancestry block/introgression tracts: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts form different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: intrinsic postmating barriers. These include both mechanical and other incompatibilities preventing egg fertilization, and hybrid inviability and/or sterility arising from incompatible combinations of genes, whereas extrinsic incompatibilities arise when trait combinations lead to reduced ecological fitness in the hybrid offspring. Pre-mating barriers: Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can occur classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. Recombination rate: Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinatorial hybrid speciation: the process by which a hybrid taxon develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. 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Hope it's ok! wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Hybridization is the process where genetically closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is an important source of novel variation. Although most hybrids are sterile or less fit than their parents, some may be survive and reproduce and enable the transfer of adaptive variants across the species boundary, or even result in the formation of novel lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number. Homoploid hybrids can sort the intrinsic barriers that isolate the parent species from each other so that a subset of these isolate the hybrid species against each parent species, or gain pre-mating extrinsic isolation from ecological differences. Hybrid species may face problems arising from incompatible combinations of genes derived from different parent species. During the process of genome stabilization selection for compatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. ==Background== Genetic exchange between species can impede biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed hybridization as maladaptive behaviour [2], which resulted can result in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary force in animals [1,6,7]. Hybridization can enrich genetic diversity of a species, lead to introgression of beneficial genetic variation, or even generate new hybrid species [1]. Hybridization is now also known to contribute to evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches [8], African ''Haplochromis'' cichlid fishes [9], ''Heliconius'' butterflies [10-12] and Hawaiian ''Madiinae'' tarweeds and silverswords [13]. Here we review the evolutionary outcomes of hybridization and the properties of genomes of hybrid species. ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If hybrids are not viable or sterile, hybridization will not affect the parent species, except perhaps for a reduction in their reproductive success [14,15]. In contrast, if the fitness of hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [16,17]; Fig. 1). If the fitness of hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [18]. Hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occassional gene flow [19,20]. In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [21,22]. Below we describe the evolutionary outcomes of hybridisation that result in hybrid genomes. [[File:Figure1 Potential evolutionary outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental specis can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from the mosquito ''Anopheles gambiae'' to ''A. coluzzii'' [20] and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta'' [23] and other ''Heliconius'' species [19]. In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from ''A. lyrata'' [24]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [25]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., a hybrid species [1,21]. A hybrid species has an admixed genome and forms stable genetically distinct populations [21]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion of a hybrid species [26], but see [27]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied homoploid hybrid species e.g. the butterfly ''Heliconius heurippa'' [10-12], the Italian sparrow ''Passer italiae'' [28], and three ''Helianthus'' sunflower species [29] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [26]. Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (introgressive speciation, c.f. [30]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinatorial hybrid speciation, [21]). A recombinant hybrid taxon typically also has a substantial proportion of the genome derived from the minority parent, although variation exist both between taxa and within lineages of hybrid taxa, see e.g. [31,32]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [27,29,33-37]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in increased ploidy compared to their parental taxa (Fig. 2). This form of hybrid speciation is more common in plants than in animals [38]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [38], but reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. [[File:Figure2 Homoploid and allopolyploid hybridization.svg|thumb|Figure 2. Shematical representation of homoploid and allopolyploid hybrid speciation.]] ===Reproductive isolation against parent species=== To successfully establish as a hybrid species, reproductive isolation against both parent species is required [1,26,39]. This reproductive isolation can arise from either intrinsic postzygotic incompatibilities frequently causing inviability or sterility, or from extrinsic ecological incompatibilities where back crosses have reduced fitness [22]. Work on ''Helianthus'' sunflowers has revealed that pre-existing structural differences [35,40], in combination with hybridization induced structural differences [35] can cause reproductive isolation against the parent species. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in the reproductively isolated Italian sparrow [28]. Ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive traits [41], or through novel combinations of ecological traits from the parent species [42]. Differences in habitat use [41] or in phenology [43] will result in some degree of reproductive isolation against parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important ecological barrier [44-47]. Premating isolation generated from assortative mating between hybrids has been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [48]. A similar pattern was found in Galapagos finches where a specific hybrid beak shape and song are thought to have been important [8], and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species [12]. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [49]. Hence, under some conditions mate choice could form important reproductive barriers to gene flow. ===Hybrid genomes and genome stabilization=== Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve indepently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behavior and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [50]. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization» (Fig. 3). Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that recombination is suppressed near genes conferring reproductive isolation [51]. The strength of the supression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [51]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes [52], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [33]. In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations [53], whereas in hybrid ''Xiphophorus'' swordtail genomes [54] genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca 2000 generations after hybridization [55], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [56]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against intrinsic incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [20,57,58]; (Fig.3). An insecticide resistance region was retained following a hybridization event in the mosquito ''A. coluzzi'' [20], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in ''Mimulus'' plants [59], in ''Mus domesticus'' house mice [60], in humans [61] and in ''Xiphophorus'' swordtail fish [31]. In addition to recombination rate, the coupling to incompatible loci may be important for the likelihood of retention of introgressed material [57]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. Schematical representation of the process of hybrid genome stabilization.]] Genome-wide incompatibilities have been identified in swordtail fish [62], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids [63] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [32,64], fungus [65] and cyto-nuclear incompatibilities in ''Mimulus'' plants [66]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [32,63,67] and genes involved in mutagenesis and cancer related pathways [63] may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations [31,54,57]. Schumer and Brandvain found that hybridization-derived regions on average are less constrained than the rest of the genome [54]. During the process of hybrid genome stabilization the minor parent genome content is overrepresented in high recombination areas, both in swordtail fish and in humans [31]. In Italian sparrows, incompatible combinations have been purged through selective retention of ancestral sites [56]. The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [68-70], to activate transposable elements [71-73], and to induce chromosomal rearrangements [74,75]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [76,77]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana'' [78]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [79]. Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization [80]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [81,82]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [82,83]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained [83]. A related allopolyploid specific phenomenon is sub genome dominance. For example, in the octoploid ''Fragaria'' strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homoeologous chromosomes are biased in favor of this subgenome, as compared with the other subgenomes [84]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [84]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissivley relative to the other subgenomes when brought together in the allopolyploid genome ([82] and [85]). Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [85]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [86,87]. Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [88]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [89], potentially buffering against a transcriptomic shock. ===In what taxa is hybridization common?=== While there is evidence for hybridization in an increasing number of taxa, sampling is not evenly distributed, and few general conclusions about the relative prevalence of hybridization can be drawn. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [90]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [91]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [92,93], and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule [94] states that "when the F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex." Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [95]. These patterns likely arise as alleles with recessive deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [96]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see [97] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [98]. This pattern may reflect the lower effective population sizes and higher suceptibility to drift on the sex chromosomes [99], the elevated frequency of loci involved in reproductive isolation [100] and/or the heightened conflict on sex chromosomes [101]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [32] is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, high rates of selfing in some species may prevent hybridization, and the breeding system may also affect the frequency of heterospecific pollen transfer [102]. Paradoxically, the ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [103]. In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae [104] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [104]. Fungal hybridization may also result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species [105]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [106], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid genome formation. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity (primary hybridization) or between divergent taxa that come into secondary contact (secondary hybridization). Secondary hybridization is expected to have a greater potential to contribute beneficial alleles or generate novelty than primary hybridization because more divergent alleles are combined in secondary hybridization and are thus more likely to have a large fitness effect or to generate transgressive phenotypes [107]. The proportion of the genome that is inherited from a minority parent varies strongly among and within species. After the initial ploidization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [108]. Relatively equal parental contributions are also found in some homoploid hybrid species [36]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [31,32]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inverted region containing genes involved in insecticide resistance [20] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly ''Heliconius numata'' [109]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [110]. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries [18,111,112], and examples include e.g. genes involved in olfaction that are introgressed across a mouse ''M. musculus'' and ''M. domesticus'' hybrid zone [113]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable us to infer what genomic regions involved in incompatibilities and reproductive isolation c.f. [114]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occassional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enable adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybridization is frequent, the advantage of novel adaptive trait combinations often override the negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last few decades have provided ample evidence that hybridization is common, contributes novel species and can enable rapid adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [33,54]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does minority parent ancestry typically remain primarily in high recombination tracts c.f. [31] or are there generally stable solutions with high contributions from both parent species across the genome c.f. [32]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. [79,108]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana [80]? Hybrid genomes, including that of many individuals of our own species [55] are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ---- ==Box: Detecting and studying hybridization with genomic tools== Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE [116], ADMIXTURE [117] or fineSTRUCTURE [118]. These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. This method can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [119]. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a the gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests [120-122] or f-statistics [123,124]. Modified versions of these tests can be used to infer introgressed genomic regions [125], the direction of gene flow [126,127] or the amount of gene flow (Reich et al. 2009). These methods can also be used to infer the relative timing of introgression with the length of the introgressed tracts [9]. For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited [128-130]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that incomplete lineage sorting and hybridization may also help [131,132]. Methods based on linkage disequilibrium decay can be used to date recent admixture events as over time ancestry tracts are continuously broken down by recombination [129,133-136]. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [137]. Demographic modeling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [138,139] or with summary statistics in an Approximate Bayesian Computation framework [140]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [141]. ---- ==Glossary== Ancestry block/introgression tracts: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts form different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: intrinsic postmating barriers. These include both mechanical and other incompatibilities preventing egg fertilization, and hybrid inviability and/or sterility arising from incompatible combinations of genes, whereas extrinsic incompatibilities arise when trait combinations lead to reduced ecological fitness in the hybrid offspring. Pre-mating barriers: Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can occur classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. Recombination rate: Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinatorial hybrid speciation: the process by which a hybrid taxon develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 g5zxfcaandwebj7i893924u8ychmsim 7573 7572 2019-04-15T14:57:08Z Eratosignis 140 /* Box: Detecting and studying hybridization with genomic tools */ Just very minor grammar edits wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Hybridization is the process where genetically closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is an important source of novel variation. Although most hybrids are sterile or less fit than their parents, some may be survive and reproduce and enable the transfer of adaptive variants across the species boundary, or even result in the formation of novel lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number. Homoploid hybrids can sort the intrinsic barriers that isolate the parent species from each other so that a subset of these isolate the hybrid species against each parent species, or gain pre-mating extrinsic isolation from ecological differences. Hybrid species may face problems arising from incompatible combinations of genes derived from different parent species. During the process of genome stabilization selection for compatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. ==Background== Genetic exchange between species can impede biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed hybridization as maladaptive behaviour [2], which resulted can result in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary force in animals [1,6,7]. Hybridization can enrich genetic diversity of a species, lead to introgression of beneficial genetic variation, or even generate new hybrid species [1]. Hybridization is now also known to contribute to evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches [8], African ''Haplochromis'' cichlid fishes [9], ''Heliconius'' butterflies [10-12] and Hawaiian ''Madiinae'' tarweeds and silverswords [13]. Here we review the evolutionary outcomes of hybridization and the properties of genomes of hybrid species. ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If hybrids are not viable or sterile, hybridization will not affect the parent species, except perhaps for a reduction in their reproductive success [14,15]. In contrast, if the fitness of hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [16,17]; Fig. 1). If the fitness of hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [18]. Hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occassional gene flow [19,20]. In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [21,22]. Below we describe the evolutionary outcomes of hybridisation that result in hybrid genomes. [[File:Figure1 Potential evolutionary outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental specis can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from the mosquito ''Anopheles gambiae'' to ''A. coluzzii'' [20] and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta'' [23] and other ''Heliconius'' species [19]. In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from ''A. lyrata'' [24]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [25]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., a hybrid species [1,21]. A hybrid species has an admixed genome and forms stable genetically distinct populations [21]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion of a hybrid species [26], but see [27]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied homoploid hybrid species e.g. the butterfly ''Heliconius heurippa'' [10-12], the Italian sparrow ''Passer italiae'' [28], and three ''Helianthus'' sunflower species [29] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [26]. Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (introgressive speciation, c.f. [30]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinatorial hybrid speciation, [21]). A recombinant hybrid taxon typically also has a substantial proportion of the genome derived from the minority parent, although variation exist both between taxa and within lineages of hybrid taxa, see e.g. [31,32]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [27,29,33-37]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in increased ploidy compared to their parental taxa (Fig. 2). This form of hybrid speciation is more common in plants than in animals [38]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [38], but reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. [[File:Figure2 Homoploid and allopolyploid hybridization.svg|thumb|Figure 2. Shematical representation of homoploid and allopolyploid hybrid speciation.]] ===Reproductive isolation against parent species=== To successfully establish as a hybrid species, reproductive isolation against both parent species is required [1,26,39]. This reproductive isolation can arise from either intrinsic postzygotic incompatibilities frequently causing inviability or sterility, or from extrinsic ecological incompatibilities where back crosses have reduced fitness [22]. Work on ''Helianthus'' sunflowers has revealed that pre-existing structural differences [35,40], in combination with hybridization induced structural differences [35] can cause reproductive isolation against the parent species. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in the reproductively isolated Italian sparrow [28]. Ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive traits [41], or through novel combinations of ecological traits from the parent species [42]. Differences in habitat use [41] or in phenology [43] will result in some degree of reproductive isolation against parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important ecological barrier [44-47]. Premating isolation generated from assortative mating between hybrids has been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [48]. A similar pattern was found in Galapagos finches where a specific hybrid beak shape and song are thought to have been important [8], and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species [12]. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [49]. Hence, under some conditions mate choice could form important reproductive barriers to gene flow. ===Hybrid genomes and genome stabilization=== Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve indepently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behavior and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [50]. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization» (Fig. 3). Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that recombination is suppressed near genes conferring reproductive isolation [51]. The strength of the supression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [51]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes [52], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [33]. In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations [53], whereas in hybrid ''Xiphophorus'' swordtail genomes [54] genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca 2000 generations after hybridization [55], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [56]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against intrinsic incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [20,57,58]; (Fig.3). An insecticide resistance region was retained following a hybridization event in the mosquito ''A. coluzzi'' [20], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in ''Mimulus'' plants [59], in ''Mus domesticus'' house mice [60], in humans [61] and in ''Xiphophorus'' swordtail fish [31]. In addition to recombination rate, the coupling to incompatible loci may be important for the likelihood of retention of introgressed material [57]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. Schematical representation of the process of hybrid genome stabilization.]] Genome-wide incompatibilities have been identified in swordtail fish [62], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids [63] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [32,64], fungus [65] and cyto-nuclear incompatibilities in ''Mimulus'' plants [66]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [32,63,67] and genes involved in mutagenesis and cancer related pathways [63] may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations [31,54,57]. Schumer and Brandvain found that hybridization-derived regions on average are less constrained than the rest of the genome [54]. During the process of hybrid genome stabilization the minor parent genome content is overrepresented in high recombination areas, both in swordtail fish and in humans [31]. In Italian sparrows, incompatible combinations have been purged through selective retention of ancestral sites [56]. The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [68-70], to activate transposable elements [71-73], and to induce chromosomal rearrangements [74,75]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [76,77]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana'' [78]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [79]. Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization [80]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [81,82]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [82,83]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained [83]. A related allopolyploid specific phenomenon is sub genome dominance. For example, in the octoploid ''Fragaria'' strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homoeologous chromosomes are biased in favor of this subgenome, as compared with the other subgenomes [84]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [84]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissivley relative to the other subgenomes when brought together in the allopolyploid genome ([82] and [85]). Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [85]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [86,87]. Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [88]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [89], potentially buffering against a transcriptomic shock. ===In what taxa is hybridization common?=== While there is evidence for hybridization in an increasing number of taxa, sampling is not evenly distributed, and few general conclusions about the relative prevalence of hybridization can be drawn. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [90]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [91]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [92,93], and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule [94] states that "when the F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex." Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [95]. These patterns likely arise as alleles with recessive deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [96]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see [97] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [98]. This pattern may reflect the lower effective population sizes and higher suceptibility to drift on the sex chromosomes [99], the elevated frequency of loci involved in reproductive isolation [100] and/or the heightened conflict on sex chromosomes [101]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [32] is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, high rates of selfing in some species may prevent hybridization, and the breeding system may also affect the frequency of heterospecific pollen transfer [102]. Paradoxically, the ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [103]. In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae [104] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [104]. Fungal hybridization may also result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species [105]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [106], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid genome formation. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity (primary hybridization) or between divergent taxa that come into secondary contact (secondary hybridization). Secondary hybridization is expected to have a greater potential to contribute beneficial alleles or generate novelty than primary hybridization because more divergent alleles are combined in secondary hybridization and are thus more likely to have a large fitness effect or to generate transgressive phenotypes [107]. The proportion of the genome that is inherited from a minority parent varies strongly among and within species. After the initial ploidization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [108]. Relatively equal parental contributions are also found in some homoploid hybrid species [36]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [31,32]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inverted region containing genes involved in insecticide resistance [20] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly ''Heliconius numata'' [109]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [110]. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries [18,111,112], and examples include e.g. genes involved in olfaction that are introgressed across a mouse ''M. musculus'' and ''M. domesticus'' hybrid zone [113]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable us to infer what genomic regions involved in incompatibilities and reproductive isolation c.f. [114]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occassional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enable adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybridization is frequent, the advantage of novel adaptive trait combinations often override the negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last few decades have provided ample evidence that hybridization is common, contributes novel species and can enable rapid adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [33,54]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does minority parent ancestry typically remain primarily in high recombination tracts c.f. [31] or are there generally stable solutions with high contributions from both parent species across the genome c.f. [32]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. [79,108]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana [80]? Hybrid genomes, including that of many individuals of our own species [55] are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ---- ==Box: Detecting and studying hybridization with genomic tools== Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE [116], ADMIXTURE [117] or fineSTRUCTURE [118]. These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. This method can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [119]. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a the gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests [120-122] or f-statistics [123,124]. Modified versions of these tests can be used to infer introgressed genomic regions [125], the direction of gene flow [126,127] or the amount of gene flow (Reich et al. 2009). These methods can also be used to infer the relative timing of introgression with the length of the introgressed tracts [9]. For datasets with a large number of taxa it may be difficult to compute all possible tests for hybridization. In such cases, graph construction methods may be better suited [128-130]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that distinguish incomplete lineage sorting and hybridization may also help [131,132]. Methods based on linkage disequilibrium decay can be used to date recent admixture events as over time ancestry tracts are continuously broken down by recombination [129,133-136]. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [137]. Demographic modeling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [138,139] or with summary statistics in an Approximate Bayesian Computation framework [140]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [141]. ---- ==Glossary== Ancestry block/introgression tracts: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts form different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: intrinsic postmating barriers. These include both mechanical and other incompatibilities preventing egg fertilization, and hybrid inviability and/or sterility arising from incompatible combinations of genes, whereas extrinsic incompatibilities arise when trait combinations lead to reduced ecological fitness in the hybrid offspring. Pre-mating barriers: Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can occur classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. Recombination rate: Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinatorial hybrid speciation: the process by which a hybrid taxon develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 61ywr3dsd5fs2mbzamgbd5b3ik9468y 7577 7573 2019-04-24T09:50:12Z RKB 141 Minor wording changes to improve precision and clarity. wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Hybridization is the process where genetically closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is an important source of novel variation. Although most hybrids are sterile or less fit than their parents, some may be survive and reproduce and enable the transfer of adaptive variants across the species boundary, or even result in the formation of novel lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number. Homoploid hybrids can sort the intrinsic barriers that isolate the parent species from each other so that a subset of these isolate the hybrid species against each parent species, or gain pre-mating extrinsic isolation from ecological differences. Hybrid species may face problems arising from incompatible combinations of genes derived from different parent species. During the process of genome stabilization selection for compatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. ==Background== Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed hybridization as maladaptive behaviour [2], which can result in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary process, contributing to increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals [1,6,7]. Hybridization can enrich genetic diversity of a species, lead to introgression of beneficial genetic variation, or even generate new hybrid species [1]. Hybridization is now also known to contribute to evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches [8], African ''Haplochromis'' cichlid fishes [9], ''Heliconius'' butterflies [10-12] and Hawaiian ''Madiinae'' tarweeds and silverswords [13]. Here we review the evolutionary outcomes of hybridization and the properties of genomes of hybrid species. ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If hybrids are not inviable or sterile, hybridization will not affect the parent species, except perhaps for a reduction in their reproductive success [14,15]. In contrast, if the fitness of hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [16,17]; Fig. 1). If the fitness of hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [18]. Hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occassional gene flow [19,20]. In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [21,22]. Below we describe the evolutionary outcomes of hybridisation that result in hybrid genomes. [[File:Figure1 Potential evolutionary outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental specis can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from the mosquito ''Anopheles gambiae'' to ''A. coluzzii'' [20] and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta'' [23] and other ''Heliconius'' species [19]. In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from ''A. lyrata'' [24]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [25]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., a hybrid species [1,21]. A hybrid species has an admixed genome and forms stable genetically distinct populations [21]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion of a hybrid species [26], but see [27]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied homoploid hybrid species e.g. the butterfly ''Heliconius heurippa'' [10-12], the Italian sparrow ''Passer italiae'' [28], and three ''Helianthus'' sunflower species [29] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [26]. Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (introgressive speciation, c.f. [30]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinatorial hybrid speciation, [21]). A recombinant hybrid taxon typically also has a substantial proportion of the genome derived from the minority parent, although variation exist both between taxa and within lineages of hybrid taxa, see e.g. [31,32]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [27,29,33-37]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in increased ploidy compared to their parental taxa (Fig. 2). This form of hybrid speciation is more common in plants than in animals [38]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [38], but reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. [[File:Figure2 Homoploid and allopolyploid hybridization.svg|thumb|Figure 2. Shematical representation of homoploid and allopolyploid hybrid speciation.]] ===Reproductive isolation against parent species=== To successfully establish as a hybrid species, reproductive isolation against both parent species is required [1,26,39]. This reproductive isolation can arise from either intrinsic postzygotic incompatibilities frequently causing inviability or sterility, or from extrinsic ecological incompatibilities where back crosses have reduced fitness [22]. Work on ''Helianthus'' sunflowers has revealed that pre-existing structural differences [35,40], in combination with hybridization induced structural differences [35] can cause reproductive isolation against the parent species. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in the reproductively isolated Italian sparrow [28]. Ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive traits [41], or through novel combinations of ecological traits from the parent species [42]. Differences in habitat use [41] or in phenology [43] will result in some degree of reproductive isolation against parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important ecological barrier [44-47]. Premating isolation generated from assortative mating between hybrids has been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [48]. A similar pattern was found in Galapagos finches where a specific hybrid beak shape and song are thought to have been important [8], and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species [12]. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [49]. Hence, under some conditions mate choice could form important reproductive barriers to gene flow. ===Hybrid genomes and genome stabilization=== Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve indepently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behavior and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [50]. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization» (Fig. 3). Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that recombination is suppressed near genes conferring reproductive isolation [51]. The strength of the supression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [51]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes [52], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [33]. In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations [53], whereas in hybrid ''Xiphophorus'' swordtail genomes [54] genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca 2000 generations after hybridization [55], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [56]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against intrinsic incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [20,57,58]; (Fig.3). An insecticide resistance region was retained following a hybridization event in the mosquito ''A. coluzzi'' [20], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in ''Mimulus'' plants [59], in ''Mus domesticus'' house mice [60], in humans [61] and in ''Xiphophorus'' swordtail fish [31]. In addition to recombination rate, the coupling to incompatible loci may be important for the likelihood of retention of introgressed material [57]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. Schematical representation of the process of hybrid genome stabilization.]] Genome-wide incompatibilities have been identified in swordtail fish [62], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids [63] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [32,64], fungus [65] and cyto-nuclear incompatibilities in ''Mimulus'' plants [66]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [32,63,67] and genes involved in mutagenesis and cancer related pathways [63] may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations [31,54,57]. Schumer and Brandvain found that hybridization-derived regions on average are less constrained than the rest of the genome [54]. During the process of hybrid genome stabilization the minor parent genome content is overrepresented in high recombination areas, both in swordtail fish and in humans [31]. In Italian sparrows, incompatible combinations have been purged through selective retention of ancestral sites [56]. The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [68-70], to activate transposable elements [71-73], and to induce chromosomal rearrangements [74,75]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [76,77]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana'' [78]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [79]. Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization [80]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [81,82]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [82,83]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained [83]. A related allopolyploid specific phenomenon is sub genome dominance. For example, in the octoploid ''Fragaria'' strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homoeologous chromosomes are biased in favor of this subgenome, as compared with the other subgenomes [84]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [84]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissivley relative to the other subgenomes when brought together in the allopolyploid genome ([82] and [85]). Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [85]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [86,87]. Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [88]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [89], potentially buffering against a transcriptomic shock. ===In what taxa is hybridization common?=== While there is evidence for hybridization in an increasing number of taxa, sampling is not evenly distributed, and few general conclusions about the relative prevalence of hybridization can be drawn. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [90]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [91]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [92,93], and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule [94] states that "when the F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex." Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [95]. These patterns likely arise as alleles with recessive deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [96]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see [97] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [98]. This pattern may reflect the lower effective population sizes and higher suceptibility to drift on the sex chromosomes [99], the elevated frequency of loci involved in reproductive isolation [100] and/or the heightened conflict on sex chromosomes [101]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [32] is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, high rates of selfing in some species may prevent hybridization, and the breeding system may also affect the frequency of heterospecific pollen transfer [102]. Paradoxically, the ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [103]. In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae [104] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [104]. Fungal hybridization may also result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species [105]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [106], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid genome formation. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity (primary hybridization) or between divergent taxa that come into secondary contact (secondary hybridization). Secondary hybridization is expected to have a greater potential to contribute beneficial alleles or generate novelty than primary hybridization because more divergent alleles are combined in secondary hybridization and are thus more likely to have a large fitness effect or to generate transgressive phenotypes [107]. The proportion of the genome that is inherited from a minority parent varies strongly among and within species. After the initial ploidization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [108]. Relatively equal parental contributions are also found in some homoploid hybrid species [36]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [31,32]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inverted region containing genes involved in insecticide resistance [20] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly ''Heliconius numata'' [109]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [110]. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries [18,111,112], and examples include e.g. genes involved in olfaction that are introgressed across a mouse ''M. musculus'' and ''M. domesticus'' hybrid zone [113]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable us to infer what genomic regions involved in incompatibilities and reproductive isolation c.f. [114]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occassional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enable adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybridization is frequent, the advantage of novel adaptive trait combinations often override the negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last few decades have provided ample evidence that hybridization is common, contributes novel species and can enable rapid adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [33,54]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does minority parent ancestry typically remain primarily in high recombination tracts c.f. [31] or are there generally stable solutions with high contributions from both parent species across the genome c.f. [32]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. [79,108]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana [80]? Hybrid genomes, including that of many individuals of our own species [55] are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ---- ==Box: Detecting and studying hybridization with genomic tools== Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE [116], ADMIXTURE [117] or fineSTRUCTURE [118]. These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. This method can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [119]. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a the gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests [120-122] or f-statistics [123,124]. Modified versions of these tests can be used to infer introgressed genomic regions [125], the direction of gene flow [126,127] or the amount of gene flow (Reich et al. 2009). These methods can also be used to infer the relative timing of introgression with the length of the introgressed tracts [9]. For datasets with a large number of taxa it may be difficult to compute all possible tests for hybridization. In such cases, graph construction methods may be better suited [128-130]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that distinguish incomplete lineage sorting and hybridization may also help [131,132]. Methods based on linkage disequilibrium decay can be used to date recent admixture events as over time ancestry tracts are continuously broken down by recombination [129,133-136]. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [137]. Demographic modeling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [138,139] or with summary statistics in an Approximate Bayesian Computation framework [140]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [141]. ---- ==Glossary== Ancestry block/introgression tracts: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts form different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: intrinsic postmating barriers. These include both mechanical and other incompatibilities preventing egg fertilization, and hybrid inviability and/or sterility arising from incompatible combinations of genes, whereas extrinsic incompatibilities arise when trait combinations lead to reduced ecological fitness in the hybrid offspring. Pre-mating barriers: Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can occur classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. Recombination rate: Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinatorial hybrid speciation: the process by which a hybrid taxon develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 t6xq29zgc5la14be62owjpbo9d87fjf 7578 7577 2019-04-26T07:25:31Z RKB 141 Minor wording changes for clarity. wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Hybridization is the process where genetically closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is an important source of novel variation. Although most hybrids are sterile or less fit than their parents, some may be survive and reproduce and enable the transfer of adaptive variants across the species boundary, or even result in the formation of novel lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number. Homoploid hybrids can sort the intrinsic barriers that isolate the parent species from each other so that a subset of these isolate the hybrid species against each parent species, or gain pre-mating extrinsic isolation from ecological differences. Hybrid species may face problems arising from incompatible combinations of genes derived from different parent species. During the process of genome stabilization selection for compatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. ==Background== Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed hybridization as maladaptive behaviour [2], which can result in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary process, contributing to increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals [1,6,7]. Hybridization can enrich genetic diversity of a species, lead to introgression of beneficial genetic variation, or even generate new hybrid species [1]. Hybridization is now also known to contribute to evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches [8], African ''Haplochromis'' cichlid fishes [9], ''Heliconius'' butterflies [10-12] and Hawaiian ''Madiinae'' tarweeds and silverswords [13]. Here we review the evolutionary outcomes of hybridization and the properties of genomes of hybrid species. ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If hybrids are not inviable or sterile, hybridization will not affect the parent species, except perhaps for a reduction in their reproductive success [14,15]. In contrast, if the fitness of hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [16,17]; Fig. 1). If the fitness of hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [18]. Hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occassional gene flow [19,20]. In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [21,22]. Below we describe the evolutionary outcomes of hybridisation that result in hybrid genomes. [[File:Figure1 Potential evolutionary outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental specis can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from the mosquito ''Anopheles gambiae'' to ''A. coluzzii'' [20] and a red warning wing colouration trait in ''Heliconius'' butterflies, which is under natural selection from predators, that has been introgressed from e.g. ''H. melpomene'' to ''H. timareta'' [23] and other ''Heliconius'' species [19]. In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from ''A. lyrata'' [24]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [25]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., a hybrid species [1,21]. A hybrid species has an admixed genome and forms stable genetically distinct populations [21]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion of a hybrid species [26], but see [27]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied homoploid hybrid species e.g. the butterfly ''Heliconius heurippa'' [10-12], the Italian sparrow ''Passer italiae'' [28], and three ''Helianthus'' sunflower species [29] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [26]. Hybrid species can occupy an ecological niche different from those of the parents and may be isolated from the parent species primarily through pre-mating barriers (introgressive speciation, c.f. [30]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinatorial hybrid speciation, [21]). A recombinant hybrid taxon typically also has a substantial proportion of the genome derived from the minority parent, although variation exists both between taxa and within lineages of hybrid taxa, see e.g. [31,32]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [27,29,33-37]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in increased ploidy compared to their parental taxa (Fig. 2). This form of hybrid speciation is more common in plants than in animals [38]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [38], but reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. [[File:Figure2 Homoploid and allopolyploid hybridization.svg|thumb|Figure 2. Shematical representation of homoploid and allopolyploid hybrid speciation.]] ===Reproductive isolation against parent species=== To establish successfully as a hybrid species, reproductive isolation against both parent species is required [1,26,39]. This reproductive isolation can arise from either intrinsic postzygotic incompatibilities frequently causing inviability or sterility, or from extrinsic ecological incompatibilities where backcrosses have reduced fitness [22]. Work on ''Helianthus'' sunflowers has revealed that pre-existing structural differences [35,40], in combination with hybridization induced structural differences [35] can cause reproductive isolation against the parent species. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in the reproductively isolated Italian sparrow [28]. Ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive traits [41], or through novel combinations of ecological traits from the parent species [42]. Differences in habitat use [41] or in phenology [43] will result in some degree of reproductive isolation against parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important ecological barrier [44-47]. Premating isolation generated from assortative mating between hybrids has been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [48]. A similar pattern was found in Galapagos finches where a specific hybrid beak shape and song are thought to have been important [8], and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species [12]. In ''Xiphophorus'' swordtail fish strong ancestry-assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [49]. Hence, under some conditions mate choice could form important reproductive barriers to gene flow. ===Hybrid genomes and genome stabilization=== Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behavior and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [50]. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization» (Fig. 3). Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that recombination is suppressed near genes conferring reproductive isolation [51]. The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [51]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes [52], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [33]. In ''Zymoseptoria'' fungi, genomes were stabilized within ca. 400 generations [53], whereas in hybrid ''Xiphophorus'' swordtail genomes [54] genome stabilization was not achieved until after ca. 2000 to 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca 2000 generations after hybridization [55], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [56]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against intrinsic incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [20,57,58]; (Fig.3). An insecticide resistance region was retained following a hybridization event in the mosquito ''A. coluzzi'' [20], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in ''Mimulus'' plants [59], in ''Mus domesticus'' house mice [60], in humans [61] and in ''Xiphophorus'' swordtail fish [31]. In addition to recombination rate, the coupling to incompatible loci may be important for the likelihood of retention of introgressed material [57]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. Schematical representation of the process of hybrid genome stabilization.|229x229px]] Genome-wide incompatibilities have been identified in swordtail fish [62], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids [63] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [32,64], fungus [65] and cyto-nuclear incompatibilities in ''Mimulus'' plants [66]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [32,63,67] and genes involved in mutagenesis and cancer related pathways [63] may cause incompatibilities in hybrids. Genome stabilization in hybrid species is shaped by selection against incompatible combinations [31,54,57]. Schumer and Brandvain found that hybridization-derived regions on average are less constrained than the rest of the genome [54]. During the process of hybrid genome stabilization the minor parent genome content is overrepresented in high recombination areas, both in swordtail fish and in humans [31]. In Italian sparrows, incompatible combinations have been purged through selective retention of ancestral sites [56]. The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [68-70], to activate transposable elements [71-73], and to induce chromosomal rearrangements [74,75]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [76,77]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana'' [78]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [79]. Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization [80]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [81,82]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [82,83]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained by selection [83]. A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid ''Fragaria'' strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homoeologous chromosomes are biased in favor of this subgenome, as compared with the other subgenomes [84]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [84]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissivley relative to the other subgenomes when brought together in the allopolyploid genome ([82] and [85]). Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [85]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [86,87]. Studies of synthetic and natural allopolyploids of ''Tragopogon miscellus'' show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [88]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [89], potentially buffering against a transcriptomic shock. ===In what taxa is hybridization common?=== While there is evidence for hybridization in an increasing number of taxa, sampling is not evenly distributed, and few general conclusions about the relative prevalence of hybridization can be drawn. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [90]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [91]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [92,93], and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule [94] states that "when the F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex." Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [95]. These patterns likely arise as alleles with recessive deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [96]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see [97] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [98]. This pattern may reflect the lower effective population sizes and higher suceptibility to drift on the sex chromosomes [99], the elevated frequency of loci involved in reproductive isolation [100] and/or the heightened conflict on sex chromosomes [101]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [32] is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, high rates of selfing in some species may prevent hybridization, and the breeding system may also affect the frequency of heterospecific pollen transfer [102]. Paradoxically, the ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [103]. In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae [104] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [104]. Fungal hybridization may also result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species [105]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [106], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid genome formation. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity (primary hybridization) or between divergent taxa that come into secondary contact (secondary hybridization). Secondary hybridization is expected to have a greater potential to contribute beneficial alleles or generate novelty than primary hybridization because more divergent alleles are combined in secondary hybridization and are thus more likely to have a large fitness effect or to generate transgressive phenotypes [107]. The proportion of the genome that is inherited from a minority parent varies strongly among and within species. After the initial ploidization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [108]. Relatively equal parental contributions are also found in some homoploid hybrid species [36]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [31,32]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inverted region containing genes involved in insecticide resistance [20] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly ''Heliconius numata'' [109]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [110]. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries [18,111,112], and examples include e.g. genes involved in olfaction that are introgressed across a mouse ''M. musculus'' and ''M. domesticus'' hybrid zone [113]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable us to infer what genomic regions involved in incompatibilities and reproductive isolation c.f. [114]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occassional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enable adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybridization is frequent, the advantage of novel adaptive trait combinations often override the negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last few decades have provided ample evidence that hybridization is common, contributes novel species and can enable rapid adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [33,54]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does minority parent ancestry typically remain primarily in high recombination tracts c.f. [31] or are there generally stable solutions with high contributions from both parent species across the genome c.f. [32]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. [79,108]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana [80]? Hybrid genomes, including that of many individuals of our own species [55] are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ---- ==Box: Detecting and studying hybridization with genomic tools== Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE [116], ADMIXTURE [117] or fineSTRUCTURE [118]. These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. This method can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [119]. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a the gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests [120-122] or f-statistics [123,124]. Modified versions of these tests can be used to infer introgressed genomic regions [125], the direction of gene flow [126,127] or the amount of gene flow (Reich et al. 2009). These methods can also be used to infer the relative timing of introgression with the length of the introgressed tracts [9]. For datasets with a large number of taxa it may be difficult to compute all possible tests for hybridization. In such cases, graph construction methods may be better suited [128-130]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that distinguish incomplete lineage sorting and hybridization may also help [131,132]. Methods based on linkage disequilibrium decay can be used to date recent admixture events as over time ancestry tracts are continuously broken down by recombination [129,133-136]. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [137]. Demographic modeling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [138,139] or with summary statistics in an Approximate Bayesian Computation framework [140]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [141]. ---- ==Glossary== Ancestry block/introgression tracts: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts form different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: intrinsic postmating barriers. These include both mechanical and other incompatibilities preventing egg fertilization, and hybrid inviability and/or sterility arising from incompatible combinations of genes, whereas extrinsic incompatibilities arise when trait combinations lead to reduced ecological fitness in the hybrid offspring. Pre-mating barriers: Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can occur classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. Recombination rate: Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinatorial hybrid speciation: the process by which a hybrid taxon develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 arype66xq3lg84xa9umqf7ao2bi20hq 7579 7578 2019-04-26T07:55:17Z RKB 141 Minor editorial points. wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Hybridization is the process where genetically closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is an important source of novel variation. Although most hybrids are sterile or less fit than their parents, some may be survive and reproduce and enable the transfer of adaptive variants across the species boundary, or even result in the formation of novel lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number. Homoploid hybrids can sort the intrinsic barriers that isolate the parent species from each other so that a subset of these isolate the hybrid species against each parent species, or gain pre-mating extrinsic isolation from ecological differences. Hybrid species may face problems arising from incompatible combinations of genes derived from different parent species. During the process of genome stabilization selection for compatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. ==Background== Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed hybridization as maladaptive behaviour [2], which can result in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary process, contributing to increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals [1,6,7]. Hybridization can enrich genetic diversity of a species, lead to introgression of beneficial genetic variation, or even generate new hybrid species [1]. Hybridization is now also known to contribute to evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches [8], African ''Haplochromis'' cichlid fishes [9], ''Heliconius'' butterflies [10-12] and Hawaiian ''Madiinae'' tarweeds and silverswords [13]. Here we review the evolutionary outcomes of hybridization and the properties of genomes of hybrid species. ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If hybrids are not inviable or sterile, hybridization will not affect the parent species, except perhaps for a reduction in their reproductive success [14,15]. In contrast, if the fitness of hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [16,17]; Fig. 1). If the fitness of hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [18]. Hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occassional gene flow [19,20]. In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [21,22]. Below we describe the evolutionary outcomes of hybridisation that result in hybrid genomes. [[File:Figure1 Potential evolutionary outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental specis can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from the mosquito ''Anopheles gambiae'' to ''A. coluzzii'' [20] and a red warning wing colouration trait in ''Heliconius'' butterflies, which is under natural selection from predators, that has been introgressed from e.g. ''H. melpomene'' to ''H. timareta'' [23] and other ''Heliconius'' species [19]. In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from ''A. lyrata'' [24]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [25]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., a hybrid species [1,21]. A hybrid species has an admixed genome and forms stable genetically distinct populations [21]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion of a hybrid species [26], but see [27]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied homoploid hybrid species e.g. the butterfly ''Heliconius heurippa'' [10-12], the Italian sparrow ''Passer italiae'' [28], and three ''Helianthus'' sunflower species [29] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [26]. Hybrid species can occupy an ecological niche different from those of the parents and may be isolated from the parent species primarily through pre-mating barriers (introgressive speciation, c.f. [30]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinatorial hybrid speciation, [21]). A recombinant hybrid taxon typically also has a substantial proportion of the genome derived from the minority parent, although variation exists both between taxa and within lineages of hybrid taxa, see e.g. [31,32]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [27,29,33-37]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in increased ploidy compared to their parental taxa (Fig. 2). This form of hybrid speciation is more common in plants than in animals [38]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [38], but reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. [[File:Figure2 Homoploid and allopolyploid hybridization.svg|thumb|Figure 2. Shematical representation of homoploid and allopolyploid hybrid speciation.]] ===Reproductive isolation against parent species=== To establish successfully as a hybrid species, reproductive isolation against both parent species is required [1,26,39]. This reproductive isolation can arise from either intrinsic postzygotic incompatibilities frequently causing inviability or sterility, or from extrinsic ecological incompatibilities where backcrosses have reduced fitness [22]. Work on ''Helianthus'' sunflowers has revealed that pre-existing structural differences [35,40], in combination with hybridization induced structural differences [35] can cause reproductive isolation against the parent species. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in the reproductively isolated Italian sparrow [28]. Ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive traits [41], or through novel combinations of ecological traits from the parent species [42]. Differences in habitat use [41] or in phenology [43] will result in some degree of reproductive isolation against parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important ecological barrier [44-47]. Premating isolation generated from assortative mating between hybrids has been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [48]. A similar pattern was found in Galapagos finches where a specific hybrid beak shape and song are thought to have been important [8], and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species [12]. In ''Xiphophorus'' swordtail fish strong ancestry-assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [49]. Hence, under some conditions mate choice could form important reproductive barriers to gene flow. ===Hybrid genomes and genome stabilization=== Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behavior and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [50]. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization» (Fig. 3). Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that recombination is suppressed near genes conferring reproductive isolation [51]. The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [51]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes [52], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [33]. In ''Zymoseptoria'' fungi, genomes were stabilized within ca. 400 generations [53], whereas in hybrid ''Xiphophorus'' swordtail genomes [54] genome stabilization was not achieved until after ca. 2000 to 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca 2000 generations after hybridization [55], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [56]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against intrinsic incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [20,57,58]; (Fig.3). An insecticide resistance region was retained following a hybridization event in the mosquito ''A. coluzzi'' [20], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in ''Mimulus'' plants [59], in ''Mus domesticus'' house mice [60], in humans [61] and in ''Xiphophorus'' swordtail fish [31]. In addition to recombination rate, the coupling to incompatible loci may be important for the likelihood of retention of introgressed material [57]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. Schematical representation of the process of hybrid genome stabilization.|229x229px]] Genome-wide incompatibilities have been identified in swordtail fish [62], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids [63] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [32,64], fungus [65] and cyto-nuclear incompatibilities in ''Mimulus'' plants [66]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [32,63,67] and genes involved in mutagenesis and cancer related pathways [63] may cause incompatibilities in hybrids. Genome stabilization in hybrid species is shaped by selection against incompatible combinations [31,54,57]. Schumer and Brandvain found that hybridization-derived regions on average are less constrained than the rest of the genome [54]. During the process of hybrid genome stabilization the minor parent genome content is overrepresented in high recombination areas, both in swordtail fish and in humans [31]. In Italian sparrows, incompatible combinations have been purged through selective retention of ancestral sites [56]. The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [68-70], to activate transposable elements [71-73], and to induce chromosomal rearrangements [74,75]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [76,77]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana'' [78]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [79]. Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization [80]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [81,82]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [82,83]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained by selection [83]. A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid ''Fragaria'' strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homoeologous chromosomes are biased in favor of this subgenome, as compared with the other subgenomes [84]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [84]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissivley relative to the other subgenomes when brought together in the allopolyploid genome ([82] and [85]). Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [85]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [86,87]. Studies of synthetic and natural allopolyploids of ''Tragopogon miscellus'' show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [88]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [89], potentially buffering against a transcriptomic shock. ===In what taxa is hybridization common?=== While there is evidence for hybridization in an increasing number of taxa, sampling is not evenly distributed, and few general conclusions about the relative prevalence of hybridization can be drawn. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [90]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [91]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [92,93], and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule [94] states that "when the F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex." Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [95]. These patterns likely arise as alleles with recessive deleterious effects in hybrids have stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [96]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has been shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY taxa (see [97] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [98]. This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes [99], the elevated frequency of loci involved in reproductive isolation [100] and/or the heightened conflict on sex chromosomes [101]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [32] is consistent with compatible sex chromosomes being important for the formation of viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, high rates of selfing in some species may prevent hybridization, and the breeding system may also affect the frequency of heterospecific pollen transfer [102]. Paradoxically, the ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [103]. In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae [104] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [104]. Fungal hybridization may also result in asexual hybrid species, as ''Epichloe'' fungi where hybrid species are asexual while nonhybrids include both asexual and sexual species [105]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [106], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid genome formation. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity (primary hybridization) or between divergent taxa that come into secondary contact (secondary hybridization). Secondary hybridization is expected to have a greater potential to contribute beneficial alleles or generate novelty than primary hybridization because more divergent alleles are combined in secondary hybridization and are thus more likely to have a large fitness effect or to generate transgressive phenotypes [107]. The proportion of the genome that is inherited from a minority parent varies strongly among and within species. After an initial polyploidization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [108]. Relatively equal parental contributions are also found in some homoploid hybrid species [36]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [31,32]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inverted region containing genes involved in insecticide resistance [20] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly ''Heliconius numata'' [109]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [110]. Genes and genomic regions that are adaptive may be readily introgressed between species, e.g. in hybrid zones, if they are not linked to incompatibility loci. This is often referred to as semi-permeable species boundaries [18,111,112], and examples include e.g. genes involved in olfaction that are introgressed across a mouse ''M. musculus'' and ''M. domesticus'' hybrid zone [113]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable us to infer what genomic regions are involved in incompatibilities and reproductive isolation c.f. [114]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species that are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enable adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybridization is frequent, the advantage of novel adaptive trait combinations can sometimes override the negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last few decades have provided ample evidence that hybridization is common, contributes novel species and can enable rapid adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [33,54]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does minority parent ancestry typically remain primarily in high recombination tracts, c.f. [31], or are there generally stable solutions with high contributions from both parent species across the genome, c.f. [32]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies, c.f. [79,108]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the ''Nicotiana'' [80]? Hybrid genomes, including those of many individuals of our own species [55] are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ---- ==Box: Detecting and studying hybridization with genomic tools== Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE [116], ADMIXTURE [117] or fineSTRUCTURE [118]. These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. This method can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [119]. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a the gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests [120-122] or f-statistics [123,124]. Modified versions of these tests can be used to infer introgressed genomic regions [125], the direction of gene flow [126,127] or the amount of gene flow (Reich et al. 2009). These methods can also be used to infer the relative timing of introgression with the length of the introgressed tracts [9]. For datasets with a large number of taxa it may be difficult to compute all possible tests for hybridization. In such cases, graph construction methods may be better suited [128-130]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that distinguish incomplete lineage sorting and hybridization may also help [131,132]. Methods based on linkage disequilibrium decay can be used to date recent admixture events as over time ancestry tracts are continuously broken down by recombination [129,133-136]. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [137]. Demographic modeling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [138,139] or with summary statistics in an Approximate Bayesian Computation framework [140]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [141]. ---- ==Glossary== Ancestry block/introgression tracts: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts form different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: intrinsic postmating barriers. These include both mechanical and other incompatibilities preventing egg fertilization, and hybrid inviability and/or sterility arising from incompatible combinations of genes, whereas extrinsic incompatibilities arise when trait combinations lead to reduced ecological fitness in the hybrid offspring. Pre-mating barriers: Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can occur classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. Recombination rate: Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinatorial hybrid speciation: the process by which a hybrid taxon develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. 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Addition of a definition for prezygotic barriers. wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Hybridization is the process where genetically closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is an important source of novel variation. Although most hybrids are sterile or less fit than their parents, some may be survive and reproduce and enable the transfer of adaptive variants across the species boundary, or even result in the formation of novel lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number. Homoploid hybrids can sort the intrinsic barriers that isolate the parent species from each other so that a subset of these isolate the hybrid species against each parent species, or gain pre-mating extrinsic isolation from ecological differences. Hybrid species may face problems arising from incompatible combinations of genes derived from different parent species. During the process of genome stabilization selection for compatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. ==Background== Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed hybridization as maladaptive behaviour [2], which can result in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary process, contributing to increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals [1,6,7]. Hybridization can enrich genetic diversity of a species, lead to introgression of beneficial genetic variation, or even generate new hybrid species [1]. Hybridization is now also known to contribute to evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches [8], African ''Haplochromis'' cichlid fishes [9], ''Heliconius'' butterflies [10-12] and Hawaiian ''Madiinae'' tarweeds and silverswords [13]. Here we review the evolutionary outcomes of hybridization and the properties of genomes of hybrid species. ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If hybrids are not inviable or sterile, hybridization will not affect the parent species, except perhaps for a reduction in their reproductive success [14,15]. In contrast, if the fitness of hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [16,17]; Fig. 1). If the fitness of hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [18]. Hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occassional gene flow [19,20]. In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [21,22]. Below we describe the evolutionary outcomes of hybridisation that result in hybrid genomes. [[File:Figure1 Potential evolutionary outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental specis can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from the mosquito ''Anopheles gambiae'' to ''A. coluzzii'' [20] and a red warning wing colouration trait in ''Heliconius'' butterflies, which is under natural selection from predators, that has been introgressed from e.g. ''H. melpomene'' to ''H. timareta'' [23] and other ''Heliconius'' species [19]. In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from ''A. lyrata'' [24]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [25]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., a hybrid species [1,21]. A hybrid species has an admixed genome and forms stable genetically distinct populations [21]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion of a hybrid species [26], but see [27]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied homoploid hybrid species e.g. the butterfly ''Heliconius heurippa'' [10-12], the Italian sparrow ''Passer italiae'' [28], and three ''Helianthus'' sunflower species [29] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [26]. Hybrid species can occupy an ecological niche different from those of the parents and may be isolated from the parent species primarily through pre-mating barriers (introgressive speciation, c.f. [30]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinatorial hybrid speciation, [21]). A recombinant hybrid taxon typically also has a substantial proportion of the genome derived from the minority parent, although variation exists both between taxa and within lineages of hybrid taxa, see e.g. [31,32]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [27,29,33-37]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in increased ploidy compared to their parental taxa (Fig. 2). This form of hybrid speciation is more common in plants than in animals [38]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [38], but reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. [[File:Figure2 Homoploid and allopolyploid hybridization.svg|thumb|Figure 2. Shematical representation of homoploid and allopolyploid hybrid speciation.]] ===Reproductive isolation against parent species=== To establish successfully as a hybrid species, reproductive isolation against both parent species is required [1,26,39]. This reproductive isolation can arise from either intrinsic postzygotic incompatibilities frequently causing inviability or sterility, or from extrinsic ecological incompatibilities where backcrosses have reduced fitness [22]. Work on ''Helianthus'' sunflowers has revealed that pre-existing structural differences [35,40], in combination with hybridization induced structural differences [35] can cause reproductive isolation against the parent species. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in the reproductively isolated Italian sparrow [28]. Ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive traits [41], or through novel combinations of ecological traits from the parent species [42]. Differences in habitat use [41] or in phenology [43] will result in some degree of reproductive isolation against parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important ecological barrier [44-47]. Premating isolation generated from assortative mating between hybrids has been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [48]. A similar pattern was found in Galapagos finches where a specific hybrid beak shape and song are thought to have been important [8], and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species [12]. In ''Xiphophorus'' swordtail fish strong ancestry-assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [49]. Hence, under some conditions mate choice could form important reproductive barriers to gene flow. ===Hybrid genomes and genome stabilization=== Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behavior and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [50]. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization» (Fig. 3). Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that recombination is suppressed near genes conferring reproductive isolation [51]. The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [51]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes [52], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [33]. In ''Zymoseptoria'' fungi, genomes were stabilized within ca. 400 generations [53], whereas in hybrid ''Xiphophorus'' swordtail genomes [54] genome stabilization was not achieved until after ca. 2000 to 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca 2000 generations after hybridization [55], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [56]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against intrinsic incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [20,57,58]; (Fig.3). An insecticide resistance region was retained following a hybridization event in the mosquito ''A. coluzzi'' [20], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in ''Mimulus'' plants [59], in ''Mus domesticus'' house mice [60], in humans [61] and in ''Xiphophorus'' swordtail fish [31]. In addition to recombination rate, the coupling to incompatible loci may be important for the likelihood of retention of introgressed material [57]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. Schematical representation of the process of hybrid genome stabilization.|229x229px]] Genome-wide incompatibilities have been identified in swordtail fish [62], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids [63] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [32,64], fungus [65] and cyto-nuclear incompatibilities in ''Mimulus'' plants [66]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [32,63,67] and genes involved in mutagenesis and cancer related pathways [63] may cause incompatibilities in hybrids. Genome stabilization in hybrid species is shaped by selection against incompatible combinations [31,54,57]. Schumer and Brandvain found that hybridization-derived regions on average are less constrained than the rest of the genome [54]. During the process of hybrid genome stabilization the minor parent genome content is overrepresented in high recombination areas, both in swordtail fish and in humans [31]. In Italian sparrows, incompatible combinations have been purged through selective retention of ancestral sites [56]. The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [68-70], to activate transposable elements [71-73], and to induce chromosomal rearrangements [74,75]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [76,77]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana'' [78]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [79]. Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization [80]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [81,82]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [82,83]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained by selection [83]. A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid ''Fragaria'' strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homoeologous chromosomes are biased in favor of this subgenome, as compared with the other subgenomes [84]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [84]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissivley relative to the other subgenomes when brought together in the allopolyploid genome ([82] and [85]). Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [85]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [86,87]. Studies of synthetic and natural allopolyploids of ''Tragopogon miscellus'' show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [88]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [89], potentially buffering against a transcriptomic shock. ===In what taxa is hybridization common?=== While there is evidence for hybridization in an increasing number of taxa, sampling is not evenly distributed, and few general conclusions about the relative prevalence of hybridization can be drawn. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [90]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [91]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [92,93], and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule [94] states that "when the F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex." Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [95]. These patterns likely arise as alleles with recessive deleterious effects in hybrids have stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [96]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has been shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY taxa (see [97] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [98]. This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes [99], the elevated frequency of loci involved in reproductive isolation [100] and/or the heightened conflict on sex chromosomes [101]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [32] is consistent with compatible sex chromosomes being important for the formation of viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, high rates of selfing in some species may prevent hybridization, and the breeding system may also affect the frequency of heterospecific pollen transfer [102]. Paradoxically, the ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [103]. In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae [104] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [104]. Fungal hybridization may also result in asexual hybrid species, as ''Epichloe'' fungi where hybrid species are asexual while nonhybrids include both asexual and sexual species [105]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [106], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid genome formation. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity (primary hybridization) or between divergent taxa that come into secondary contact (secondary hybridization). Secondary hybridization is expected to have a greater potential to contribute beneficial alleles or generate novelty than primary hybridization because more divergent alleles are combined in secondary hybridization and are thus more likely to have a large fitness effect or to generate transgressive phenotypes [107]. The proportion of the genome that is inherited from a minority parent varies strongly among and within species. After an initial polyploidization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [108]. Relatively equal parental contributions are also found in some homoploid hybrid species [36]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [31,32]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inverted region containing genes involved in insecticide resistance [20] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly ''Heliconius numata'' [109]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [110]. Genes and genomic regions that are adaptive may be readily introgressed between species, e.g. in hybrid zones, if they are not linked to incompatibility loci. This is often referred to as semi-permeable species boundaries [18,111,112], and examples include e.g. genes involved in olfaction that are introgressed across a mouse ''M. musculus'' and ''M. domesticus'' hybrid zone [113]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable us to infer what genomic regions are involved in incompatibilities and reproductive isolation c.f. [114]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species that are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enable adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybridization is frequent, the advantage of novel adaptive trait combinations can sometimes override the negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last few decades have provided ample evidence that hybridization is common, contributes novel species and can enable rapid adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [33,54]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does minority parent ancestry typically remain primarily in high recombination tracts, c.f. [31], or are there generally stable solutions with high contributions from both parent species across the genome, c.f. [32]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies, c.f. [79,108]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the ''Nicotiana'' [80]? Hybrid genomes, including those of many individuals of our own species [55] are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ---- ==Box: Detecting and studying hybridization with genomic tools== Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE [116], ADMIXTURE [117] or fineSTRUCTURE [118]. These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. This method can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [119]. If genomic data of multiple species are available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a the gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods has been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statistics or ABBA-BABA tests [120-122] or f-statistics [123,124]. Modified versions of these tests can be used to infer introgressed genomic regions [125], the direction of gene flow [126,127] or the amount of gene flow (Reich et al. 2009). These methods can also be used to infer the relative timing of introgression with the length of the introgressed tracts [9]. For datasets with a large number of taxa it may be difficult to compute all possible tests for hybridization. In such cases, graph construction methods may be better suited [128-130]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that distinguish incomplete lineage sorting and hybridization may also help [131,132]. Methods based on linkage disequilibrium decay can be used to date recent admixture events as over time ancestry tracts are continuously broken down by recombination [129,133-136]. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [137]. Demographic modeling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [138,139] or with summary statistics in an Approximate Bayesian Computation framework [140]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [141]. ---- ==Glossary== Ancestry block/introgression tract: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts form different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random inheritance of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through mutation, drift, gene flow or selection. It is broken down recombination and so is often strong between genes that are physically linked, i.e. residing on the same chromosome. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: reproductive barriers operating after zygote formation. These include intrinsic hybrid inviability and/or sterility arising from incompatible combinations of genes, and extrinsic incompatibilities that arise when trait combinations lead to reduced ecological fitness in the hybrid offspring. Prezygotic barriers: premating barrier and also mechanical and other incompatibilities preventing egg fertilization Pre-mating barriers: factors that make individuals more likely to mate with members of their own population than of another population or prevent mating between the populations. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending on whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring independent of the environment or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against in particular environments. Recombination rate: recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinatorial hybrid speciation: the process by which a hybrid taxon develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. Transgressive segregation: extreme phenotypes in hybrids, outside the range of trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] =References= <references /> [[Category:PLOS Genetics drafts]] 1. Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, et al. Hybridization and speciation. J Evol Biol. 2013;26: 229–246. doi:10.1111/j.1420-9101.2012.02599.x 2. Fisher RA. The genetical theory of natural selection. Oxford: Clarendon Press; 1930. doi:10.5962/bhl.title.27468 3. Mayr E. Animal Species and Evolution. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 bq2cya96is5k0o5v66enk824zsj12ty 7779 7580 2019-06-29T08:25:04Z Annarunemark 132 /* Abstract */ wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is common, and that it may represent an important source of novel variation. Although most interspecific hybrids are sterile or less fit than their parents, some may survive and reproduce, enabling the transfer of adaptive variants across the species boundary, and even result in the formation of novel evolutionary lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel ecological niches, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. The potential for rapid adapation or speciation makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how introgressed alleles or hybrid species can establish and how the resulting hybrid genomes evolve. ==Background== Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed hybridization as maladaptive behaviour [2], which can result in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary process, contributing to increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals [1,6,7]. Hybridization can enrich genetic diversity of a species, lead to introgression of beneficial genetic variation, or even generate new hybrid species [1]. Hybridization is now also known to contribute to evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches [8], African ''Haplochromis'' cichlid fishes [9], ''Heliconius'' butterflies [10-12] and Hawaiian ''Madiinae'' tarweeds and silverswords [13]. Here we review the evolutionary outcomes of hybridization and the properties of genomes of hybrid species. ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If hybrids are not inviable or sterile, hybridization will not affect the parent species, except perhaps for a reduction in their reproductive success [14,15]. In contrast, if the fitness of hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [16,17]; Fig. 1). If the fitness of hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [18]. Hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occassional gene flow [19,20]. In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [21,22]. Below we describe the evolutionary outcomes of hybridisation that result in hybrid genomes. [[File:Figure1 Potential evolutionary outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental specis can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from the mosquito ''Anopheles gambiae'' to ''A. coluzzii'' [20] and a red warning wing colouration trait in ''Heliconius'' butterflies, which is under natural selection from predators, that has been introgressed from e.g. ''H. melpomene'' to ''H. timareta'' [23] and other ''Heliconius'' species [19]. In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from ''A. lyrata'' [24]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [25]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., a hybrid species [1,21]. A hybrid species has an admixed genome and forms stable genetically distinct populations [21]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion of a hybrid species [26], but see [27]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied homoploid hybrid species e.g. the butterfly ''Heliconius heurippa'' [10-12], the Italian sparrow ''Passer italiae'' [28], and three ''Helianthus'' sunflower species [29] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [26]. Hybrid species can occupy an ecological niche different from those of the parents and may be isolated from the parent species primarily through pre-mating barriers (introgressive speciation, c.f. [30]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinatorial hybrid speciation, [21]). A recombinant hybrid taxon typically also has a substantial proportion of the genome derived from the minority parent, although variation exists both between taxa and within lineages of hybrid taxa, see e.g. [31,32]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [27,29,33-37]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in increased ploidy compared to their parental taxa (Fig. 2). This form of hybrid speciation is more common in plants than in animals [38]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [38], but reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. [[File:Figure2 Homoploid and allopolyploid hybridization.svg|thumb|Figure 2. Shematical representation of homoploid and allopolyploid hybrid speciation.]] ===Reproductive isolation against parent species=== To establish successfully as a hybrid species, reproductive isolation against both parent species is required [1,26,39]. This reproductive isolation can arise from either intrinsic postzygotic incompatibilities frequently causing inviability or sterility, or from extrinsic ecological incompatibilities where backcrosses have reduced fitness [22]. Work on ''Helianthus'' sunflowers has revealed that pre-existing structural differences [35,40], in combination with hybridization induced structural differences [35] can cause reproductive isolation against the parent species. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in the reproductively isolated Italian sparrow [28]. Ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive traits [41], or through novel combinations of ecological traits from the parent species [42]. Differences in habitat use [41] or in phenology [43] will result in some degree of reproductive isolation against parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important ecological barrier [44-47]. Premating isolation generated from assortative mating between hybrids has been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [48]. A similar pattern was found in Galapagos finches where a specific hybrid beak shape and song are thought to have been important [8], and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species [12]. In ''Xiphophorus'' swordtail fish strong ancestry-assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [49]. Hence, under some conditions mate choice could form important reproductive barriers to gene flow. ===Hybrid genomes and genome stabilization=== Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behavior and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [50]. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization» (Fig. 3). Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that recombination is suppressed near genes conferring reproductive isolation [51]. The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [51]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes [52], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [33]. In ''Zymoseptoria'' fungi, genomes were stabilized within ca. 400 generations [53], whereas in hybrid ''Xiphophorus'' swordtail genomes [54] genome stabilization was not achieved until after ca. 2000 to 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca 2000 generations after hybridization [55], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [56]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against intrinsic incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [20,57,58]; (Fig.3). An insecticide resistance region was retained following a hybridization event in the mosquito ''A. coluzzi'' [20], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in ''Mimulus'' plants [59], in ''Mus domesticus'' house mice [60], in humans [61] and in ''Xiphophorus'' swordtail fish [31]. In addition to recombination rate, the coupling to incompatible loci may be important for the likelihood of retention of introgressed material [57]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. Schematical representation of the process of hybrid genome stabilization.|229x229px]] Genome-wide incompatibilities have been identified in swordtail fish [62], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids [63] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [32,64], fungus [65] and cyto-nuclear incompatibilities in ''Mimulus'' plants [66]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [32,63,67] and genes involved in mutagenesis and cancer related pathways [63] may cause incompatibilities in hybrids. Genome stabilization in hybrid species is shaped by selection against incompatible combinations [31,54,57]. Schumer and Brandvain found that hybridization-derived regions on average are less constrained than the rest of the genome [54]. During the process of hybrid genome stabilization the minor parent genome content is overrepresented in high recombination areas, both in swordtail fish and in humans [31]. In Italian sparrows, incompatible combinations have been purged through selective retention of ancestral sites [56]. The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [68-70], to activate transposable elements [71-73], and to induce chromosomal rearrangements [74,75]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [76,77]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana'' [78]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [79]. Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization [80]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [81,82]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [82,83]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained by selection [83]. A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid ''Fragaria'' strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homoeologous chromosomes are biased in favor of this subgenome, as compared with the other subgenomes [84]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [84]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissivley relative to the other subgenomes when brought together in the allopolyploid genome ([82] and [85]). Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [85]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [86,87]. Studies of synthetic and natural allopolyploids of ''Tragopogon miscellus'' show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [88]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [89], potentially buffering against a transcriptomic shock. ===In what taxa is hybridization common?=== While there is evidence for hybridization in an increasing number of taxa, sampling is not evenly distributed, and few general conclusions about the relative prevalence of hybridization can be drawn. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [90]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [91]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [92,93], and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule [94] states that "when the F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex." Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [95]. These patterns likely arise as alleles with recessive deleterious effects in hybrids have stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [96]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has been shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY taxa (see [97] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [98]. This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes [99], the elevated frequency of loci involved in reproductive isolation [100] and/or the heightened conflict on sex chromosomes [101]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [32] is consistent with compatible sex chromosomes being important for the formation of viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, high rates of selfing in some species may prevent hybridization, and the breeding system may also affect the frequency of heterospecific pollen transfer [102]. Paradoxically, the ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [103]. In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae [104] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [104]. Fungal hybridization may also result in asexual hybrid species, as ''Epichloe'' fungi where hybrid species are asexual while nonhybrids include both asexual and sexual species [105]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [106], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid genome formation. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity (primary hybridization) or between divergent taxa that come into secondary contact (secondary hybridization). Secondary hybridization is expected to have a greater potential to contribute beneficial alleles or generate novelty than primary hybridization because more divergent alleles are combined in secondary hybridization and are thus more likely to have a large fitness effect or to generate transgressive phenotypes [107]. The proportion of the genome that is inherited from a minority parent varies strongly among and within species. After an initial polyploidization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [108]. Relatively equal parental contributions are also found in some homoploid hybrid species [36]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [31,32]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inverted region containing genes involved in insecticide resistance [20] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly ''Heliconius numata'' [109]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [110]. Genes and genomic regions that are adaptive may be readily introgressed between species, e.g. in hybrid zones, if they are not linked to incompatibility loci. This is often referred to as semi-permeable species boundaries [18,111,112], and examples include e.g. genes involved in olfaction that are introgressed across a mouse ''M. musculus'' and ''M. domesticus'' hybrid zone [113]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable us to infer what genomic regions are involved in incompatibilities and reproductive isolation c.f. [114]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species that are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enable adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybridization is frequent, the advantage of novel adaptive trait combinations can sometimes override the negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last few decades have provided ample evidence that hybridization is common, contributes novel species and can enable rapid adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [33,54]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does minority parent ancestry typically remain primarily in high recombination tracts, c.f. [31], or are there generally stable solutions with high contributions from both parent species across the genome, c.f. [32]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies, c.f. [79,108]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the ''Nicotiana'' [80]? Hybrid genomes, including those of many individuals of our own species [55] are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ---- ==Box: Detecting and studying hybridization with genomic tools== Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE [116], ADMIXTURE [117] or fineSTRUCTURE [118]. These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. This method can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [119]. If genomic data of multiple species are available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a the gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods has been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statistics or ABBA-BABA tests [120-122] or f-statistics [123,124]. Modified versions of these tests can be used to infer introgressed genomic regions [125], the direction of gene flow [126,127] or the amount of gene flow (Reich et al. 2009). These methods can also be used to infer the relative timing of introgression with the length of the introgressed tracts [9]. For datasets with a large number of taxa it may be difficult to compute all possible tests for hybridization. In such cases, graph construction methods may be better suited [128-130]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that distinguish incomplete lineage sorting and hybridization may also help [131,132]. Methods based on linkage disequilibrium decay can be used to date recent admixture events as over time ancestry tracts are continuously broken down by recombination [129,133-136]. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [137]. Demographic modeling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [138,139] or with summary statistics in an Approximate Bayesian Computation framework [140]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [141]. ---- ==Glossary== Ancestry block/introgression tract: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts form different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random inheritance of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through mutation, drift, gene flow or selection. It is broken down recombination and so is often strong between genes that are physically linked, i.e. residing on the same chromosome. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: reproductive barriers operating after zygote formation. These include intrinsic hybrid inviability and/or sterility arising from incompatible combinations of genes, and extrinsic incompatibilities that arise when trait combinations lead to reduced ecological fitness in the hybrid offspring. Prezygotic barriers: premating barrier and also mechanical and other incompatibilities preventing egg fertilization Pre-mating barriers: factors that make individuals more likely to mate with members of their own population than of another population or prevent mating between the populations. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending on whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring independent of the environment or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against in particular environments. Recombination rate: recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinatorial hybrid speciation: the process by which a hybrid taxon develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. Transgressive segregation: extreme phenotypes in hybrids, outside the range of trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] =References= <references /> [[Category:PLOS Genetics drafts]] 1. Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, et al. Hybridization and speciation. J Evol Biol. 2013;26: 229–246. doi:10.1111/j.1420-9101.2012.02599.x 2. Fisher RA. The genetical theory of natural selection. Oxford: Clarendon Press; 1930. doi:10.5962/bhl.title.27468 3. Mayr E. Animal Species and Evolution. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 j73pn0nyxt6jyh2zb5t6pslo4hjhd9t 7780 7779 2019-06-29T09:18:17Z Annarunemark 132 /* Background */ wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is common, and that it may represent an important source of novel variation. Although most interspecific hybrids are sterile or less fit than their parents, some may survive and reproduce, enabling the transfer of adaptive variants across the species boundary, and even result in the formation of novel evolutionary lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel ecological niches, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. The potential for rapid adapation or speciation makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how introgressed alleles or hybrid species can establish and how the resulting hybrid genomes evolve. ==Background== Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour [2] which can result in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals [1,6,7]. Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species [1]. Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the Geospiza Galapagos finches [8], African cichlid fishes [9], Heliconius butterflies [10-12] and Hawaiian Madiinae tarweeds and silverswords [13]. Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species [14,15]. This could potentially lead to reinforcement, selection to strengthen premating isolation [16] or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort [14]. If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [17,18]; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [19]. If hybrids are fertile, hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable neutral or selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occasional gene flow [20,21]. Hybrid fitness may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including Drosophila [22], birds [23] and fish [24]. Hybrid fitness may also differ with cross direction [25], between first generation and later generation hybrids [26], and among individuals within generations of the same cross-type [27,28] . In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [29,30]. Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3 Potential outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial [1]. Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced [31,32], or the adaptive loci are tightly linked to deleterious ones [33]. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from Anopheles gambiae to A. coluzzii [21] and the red warning wing colouration trait in Heliconius butterflies that is under natural selection from predators which has been introgressed from e.g. H. melpomene to H. timareta [34] and other Heliconius species [20]. In the plant Arabidopsis arenosa some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from A. lyrata [35]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [36]. If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolatated against other populations of the same species. Examples of this include Heliconius butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g. [37]), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between H. t. florencia and H. t. linaresi) and intermediate levels (e.g. H. c. galanthus/H. pachinus) of divergence [38]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation [1,29]. A hybrid species has an admixed genome and forms stable genetically distinct populations [29]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation [39], but see [40]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. Heliconius heurippa [10-12], Passer italiae [28], and three Helianthus sunflower species [41] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [39]. Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. [42]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation, [29]). A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exist both between taxa and within lineages of hybrid taxa, see e.g. [43,44]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [40,41,45-49]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an allopolyploid with increased ploidy compared to their parental taxa (Fig. 2). ). In contrast to allopolyploids, autopolyploids are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals [50]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [50]. [[File:Figure2 Homoploid and allopolyploid hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] ===Reproductive isolation against parent species=== Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species [1,39,51]. Reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental condictions (extrinsic or intrinsic barriers, respectively) [52] . For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments [30]. Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier [53-56]. Strong extrinsic pre-zygotic have been shown to isolate the hybrid species Senecio eboracensis from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments [57]. Lowe & Abbott [57] conclude that selfing, timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation. Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [58]. A similar pattern was found in Geospiza Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology [8], and hybrid Heliconius butterflies preferred the hybrid wing patterning over that of both parent species [12]. Intrinsic differences in habitat use [59] or in phenology [60] may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in Rhagoletis pomonella maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple [61,62] and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In Xiphophorus swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [63]. Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on Helianthus sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences [47,64], in combination with hybridization induced structural differences [47]. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow Passer italiae and its parent species [28]. Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species[65], the population size of the hybrid species[66], the nature of selection acting on hybrids, and linkage among incompatibilities to each other and to adaptive variants [67]. Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive phenotypes [59], or through novel combinations of ecological traits from the parent species [68], and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. ===Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [69] as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization»[45]. Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids [70]. The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [70]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid Helianthus sunflower species genomes [71], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [45]. In Zymoseptoria fungi genomes were stabilized within ca. 400 generations [72], whereas in hybrid Xiphophorus swordtail genomes [73] genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization [74], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [75]. Given time, genetic drift will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations [45]. Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in that hybrids retaining both parental alleles and hence are not homozygous for any weakly deleterious alleles have higher fitness than homozygous hybrids. This associative overdominance [76,77], may slow down the process of fixation of parental alleles through favouring retention of both parental alleles. The effect of assortative overdominance is strongest in low recombination regions, including inversions [78]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [21,79,80]; (Fig.3). An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi [21], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus [81], in Mus domesticus house mice [82], in Heliconius butterflies [80] and in Xiphophorus swordtail fish [43]. Genome-wide incompatibilities have been identified in Xipophorous fish [83], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids [84] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [49,85], fungus [86] and cyto-nuclear incompatibilities in Mimulus plants [87]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [49,84,88] and genes involved in mutagenesis and cancer related pathways [84] may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations [43,73,79]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.|229x229px]] ===Altered genome properties in hybrid taxa=== The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [52,89,90], to activate transposable elements [91-93], and to induce chromosomal rearrangements [94,95]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [96,97]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana [98]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [99]. Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization [100]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [101,102]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [102,103]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained [103]. A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes [104]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [104]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome [102],[105]. Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [105]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [106,107]. Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [108]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [109], potentially buffering against a transcriptomic shock. ===What factors influence the likelihood of the formation of persistent hybrid genomes?=== Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [110]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [111]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [112,113], and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule [114] states that when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [22]. These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [115]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see [116] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [117]. This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes [118], the elevated frequency of loci involved in reproductive isolation [119] and/or the heightened conflict on sex chromosomes [120]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [49] is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer [121][122]. In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae [123] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [123]. For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [124]. Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study [125], and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species [126]. Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis [127], and most if not all asexual vertebrate species are of hybrid origin [128]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [129], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes [130]. In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies[34]. Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes [131]. Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness [132] but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above [131]. An intermediate genetic distance may thus be most condusive to hybrid speciation [131]. Experimental lab crosses support this hypothesis [65]. The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [133]. Relatively equal parental contributions are also found in some homoploid hybrid species [48] but in other cases they are highly unequal such as in some Heliconius species [134]. The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes [135]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [43,44]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance [21] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata [136]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [137]. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries [19,138,139], and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone [140]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. [141]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [45,73]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. [43] or are there generally stable solutions with high contributions from both parent species across the genome c.f. [49]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. [99,133]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana [100]? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ===References=== 1. 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These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. This method can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [119]. If genomic data of multiple species are available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a the gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods has been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statistics or ABBA-BABA tests [120-122] or f-statistics [123,124]. Modified versions of these tests can be used to infer introgressed genomic regions [125], the direction of gene flow [126,127] or the amount of gene flow (Reich et al. 2009). These methods can also be used to infer the relative timing of introgression with the length of the introgressed tracts [9]. For datasets with a large number of taxa it may be difficult to compute all possible tests for hybridization. In such cases, graph construction methods may be better suited [128-130]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that distinguish incomplete lineage sorting and hybridization may also help [131,132]. Methods based on linkage disequilibrium decay can be used to date recent admixture events as over time ancestry tracts are continuously broken down by recombination [129,133-136]. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [137]. Demographic modeling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [138,139] or with summary statistics in an Approximate Bayesian Computation framework [140]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [141]. ---- ==Glossary== Ancestry block/introgression tract: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts form different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random inheritance of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through mutation, drift, gene flow or selection. It is broken down recombination and so is often strong between genes that are physically linked, i.e. residing on the same chromosome. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: reproductive barriers operating after zygote formation. These include intrinsic hybrid inviability and/or sterility arising from incompatible combinations of genes, and extrinsic incompatibilities that arise when trait combinations lead to reduced ecological fitness in the hybrid offspring. Prezygotic barriers: premating barrier and also mechanical and other incompatibilities preventing egg fertilization Pre-mating barriers: factors that make individuals more likely to mate with members of their own population than of another population or prevent mating between the populations. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending on whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring independent of the environment or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against in particular environments. Recombination rate: recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinatorial hybrid speciation: the process by which a hybrid taxon develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. Transgressive segregation: extreme phenotypes in hybrids, outside the range of trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] =References= <references /> [[Category:PLOS Genetics drafts]] 1. Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, et al. Hybridization and speciation. J Evol Biol. 2013;26: 229–246. doi:10.1111/j.1420-9101.2012.02599.x 2. Fisher RA. The genetical theory of natural selection. Oxford: Clarendon Press; 1930. doi:10.5962/bhl.title.27468 3. Mayr E. Animal Species and Evolution. Cambridge, MA and London, England: Harvard University Press; 1963. doi:10.4159/harvard.9780674865327 4. Stebbins GL. The Role of Hybridization in Evolution. Proc. Am. Philos. Soc. 1959;103: 231–251. 5. Andersson E, Stebbins GL. Hybridization as an evolutionary stimulus. Evolution. 1954;4: 378–388. 6. Arnold ML. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 f2j7pmbzzxjt2xbyx24ccu73pvsgrw2 7781 7780 2019-06-29T09:19:36Z Annarunemark 132 /* Box: Detecting and studying hybridization with genomic tools */ wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is common, and that it may represent an important source of novel variation. Although most interspecific hybrids are sterile or less fit than their parents, some may survive and reproduce, enabling the transfer of adaptive variants across the species boundary, and even result in the formation of novel evolutionary lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel ecological niches, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. The potential for rapid adapation or speciation makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how introgressed alleles or hybrid species can establish and how the resulting hybrid genomes evolve. ==Background== Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour [2] which can result in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals [1,6,7]. Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species [1]. Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the Geospiza Galapagos finches [8], African cichlid fishes [9], Heliconius butterflies [10-12] and Hawaiian Madiinae tarweeds and silverswords [13]. Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species [14,15]. This could potentially lead to reinforcement, selection to strengthen premating isolation [16] or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort [14]. If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [17,18]; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [19]. If hybrids are fertile, hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable neutral or selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occasional gene flow [20,21]. Hybrid fitness may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including Drosophila [22], birds [23] and fish [24]. Hybrid fitness may also differ with cross direction [25], between first generation and later generation hybrids [26], and among individuals within generations of the same cross-type [27,28] . In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [29,30]. Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3 Potential outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial [1]. Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced [31,32], or the adaptive loci are tightly linked to deleterious ones [33]. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from Anopheles gambiae to A. coluzzii [21] and the red warning wing colouration trait in Heliconius butterflies that is under natural selection from predators which has been introgressed from e.g. H. melpomene to H. timareta [34] and other Heliconius species [20]. In the plant Arabidopsis arenosa some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from A. lyrata [35]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [36]. If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolatated against other populations of the same species. Examples of this include Heliconius butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g. [37]), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between H. t. florencia and H. t. linaresi) and intermediate levels (e.g. H. c. galanthus/H. pachinus) of divergence [38]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation [1,29]. A hybrid species has an admixed genome and forms stable genetically distinct populations [29]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation [39], but see [40]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. Heliconius heurippa [10-12], Passer italiae [28], and three Helianthus sunflower species [41] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [39]. Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. [42]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation, [29]). A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exist both between taxa and within lineages of hybrid taxa, see e.g. [43,44]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [40,41,45-49]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an allopolyploid with increased ploidy compared to their parental taxa (Fig. 2). ). In contrast to allopolyploids, autopolyploids are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals [50]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [50]. [[File:Figure2 Homoploid and allopolyploid hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] ===Reproductive isolation against parent species=== Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species [1,39,51]. Reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental condictions (extrinsic or intrinsic barriers, respectively) [52] . For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments [30]. Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier [53-56]. Strong extrinsic pre-zygotic have been shown to isolate the hybrid species Senecio eboracensis from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments [57]. Lowe & Abbott [57] conclude that selfing, timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation. Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [58]. A similar pattern was found in Geospiza Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology [8], and hybrid Heliconius butterflies preferred the hybrid wing patterning over that of both parent species [12]. Intrinsic differences in habitat use [59] or in phenology [60] may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in Rhagoletis pomonella maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple [61,62] and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In Xiphophorus swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [63]. Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on Helianthus sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences [47,64], in combination with hybridization induced structural differences [47]. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow Passer italiae and its parent species [28]. Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species[65], the population size of the hybrid species[66], the nature of selection acting on hybrids, and linkage among incompatibilities to each other and to adaptive variants [67]. Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive phenotypes [59], or through novel combinations of ecological traits from the parent species [68], and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. ===Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [69] as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization»[45]. Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids [70]. The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [70]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid Helianthus sunflower species genomes [71], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [45]. In Zymoseptoria fungi genomes were stabilized within ca. 400 generations [72], whereas in hybrid Xiphophorus swordtail genomes [73] genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization [74], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [75]. Given time, genetic drift will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations [45]. Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in that hybrids retaining both parental alleles and hence are not homozygous for any weakly deleterious alleles have higher fitness than homozygous hybrids. This associative overdominance [76,77], may slow down the process of fixation of parental alleles through favouring retention of both parental alleles. The effect of assortative overdominance is strongest in low recombination regions, including inversions [78]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [21,79,80]; (Fig.3). An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi [21], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus [81], in Mus domesticus house mice [82], in Heliconius butterflies [80] and in Xiphophorus swordtail fish [43]. Genome-wide incompatibilities have been identified in Xipophorous fish [83], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids [84] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [49,85], fungus [86] and cyto-nuclear incompatibilities in Mimulus plants [87]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [49,84,88] and genes involved in mutagenesis and cancer related pathways [84] may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations [43,73,79]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.|229x229px]] ===Altered genome properties in hybrid taxa=== The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [52,89,90], to activate transposable elements [91-93], and to induce chromosomal rearrangements [94,95]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [96,97]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana [98]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [99]. Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization [100]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [101,102]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [102,103]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained [103]. A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes [104]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [104]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome [102],[105]. Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [105]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [106,107]. Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [108]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [109], potentially buffering against a transcriptomic shock. ===What factors influence the likelihood of the formation of persistent hybrid genomes?=== Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [110]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [111]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [112,113], and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule [114] states that when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [22]. These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [115]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see [116] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [117]. This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes [118], the elevated frequency of loci involved in reproductive isolation [119] and/or the heightened conflict on sex chromosomes [120]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [49] is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer [121][122]. In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae [123] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [123]. For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [124]. Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study [125], and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species [126]. Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis [127], and most if not all asexual vertebrate species are of hybrid origin [128]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [129], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes [130]. In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies[34]. Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes [131]. Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness [132] but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above [131]. An intermediate genetic distance may thus be most condusive to hybrid speciation [131]. Experimental lab crosses support this hypothesis [65]. The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [133]. Relatively equal parental contributions are also found in some homoploid hybrid species [48] but in other cases they are highly unequal such as in some Heliconius species [134]. The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes [135]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [43,44]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance [21] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata [136]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [137]. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries [19,138,139], and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone [140]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. [141]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [45,73]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. [43] or are there generally stable solutions with high contributions from both parent species across the genome c.f. [49]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. [99,133]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana [100]? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ===References=== 1. 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These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [146]. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests [147-149] or f-statistics [150,151]. Modified versions of these tests can be used to infer introgressed genomic regions [152], the direction of gene flow [153,154] or the amount of gene flow [151]. For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited [155-157]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help [158,159]. Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination [156,160-163]. With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [164]. Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [165,166] or with summary statistics in an Approximate Bayesian Computation framework [167]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [168].  ---- ==Glossary== Ancestry block/introgression tract: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts form different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random inheritance of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through mutation, drift, gene flow or selection. It is broken down recombination and so is often strong between genes that are physically linked, i.e. residing on the same chromosome. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: reproductive barriers operating after zygote formation. These include intrinsic hybrid inviability and/or sterility arising from incompatible combinations of genes, and extrinsic incompatibilities that arise when trait combinations lead to reduced ecological fitness in the hybrid offspring. Prezygotic barriers: premating barrier and also mechanical and other incompatibilities preventing egg fertilization Pre-mating barriers: factors that make individuals more likely to mate with members of their own population than of another population or prevent mating between the populations. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending on whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring independent of the environment or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against in particular environments. Recombination rate: recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 6x7ndr7jq6l97l7vz5zyxvwwepo8393 7782 7781 2019-06-29T09:20:06Z Annarunemark 132 /* Glossary */ wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is common, and that it may represent an important source of novel variation. Although most interspecific hybrids are sterile or less fit than their parents, some may survive and reproduce, enabling the transfer of adaptive variants across the species boundary, and even result in the formation of novel evolutionary lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel ecological niches, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. The potential for rapid adapation or speciation makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how introgressed alleles or hybrid species can establish and how the resulting hybrid genomes evolve. ==Background== Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour [2] which can result in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals [1,6,7]. Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species [1]. Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the Geospiza Galapagos finches [8], African cichlid fishes [9], Heliconius butterflies [10-12] and Hawaiian Madiinae tarweeds and silverswords [13]. Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species [14,15]. This could potentially lead to reinforcement, selection to strengthen premating isolation [16] or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort [14]. If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [17,18]; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [19]. If hybrids are fertile, hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable neutral or selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occasional gene flow [20,21]. Hybrid fitness may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including Drosophila [22], birds [23] and fish [24]. Hybrid fitness may also differ with cross direction [25], between first generation and later generation hybrids [26], and among individuals within generations of the same cross-type [27,28] . In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [29,30]. Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3 Potential outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial [1]. Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced [31,32], or the adaptive loci are tightly linked to deleterious ones [33]. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from Anopheles gambiae to A. coluzzii [21] and the red warning wing colouration trait in Heliconius butterflies that is under natural selection from predators which has been introgressed from e.g. H. melpomene to H. timareta [34] and other Heliconius species [20]. In the plant Arabidopsis arenosa some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from A. lyrata [35]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [36]. If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolatated against other populations of the same species. Examples of this include Heliconius butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g. [37]), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between H. t. florencia and H. t. linaresi) and intermediate levels (e.g. H. c. galanthus/H. pachinus) of divergence [38]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation [1,29]. A hybrid species has an admixed genome and forms stable genetically distinct populations [29]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation [39], but see [40]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. Heliconius heurippa [10-12], Passer italiae [28], and three Helianthus sunflower species [41] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [39]. Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. [42]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation, [29]). A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exist both between taxa and within lineages of hybrid taxa, see e.g. [43,44]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [40,41,45-49]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an allopolyploid with increased ploidy compared to their parental taxa (Fig. 2). ). In contrast to allopolyploids, autopolyploids are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals [50]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [50]. [[File:Figure2 Homoploid and allopolyploid hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] ===Reproductive isolation against parent species=== Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species [1,39,51]. Reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental condictions (extrinsic or intrinsic barriers, respectively) [52] . For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments [30]. Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier [53-56]. Strong extrinsic pre-zygotic have been shown to isolate the hybrid species Senecio eboracensis from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments [57]. Lowe & Abbott [57] conclude that selfing, timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation. Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [58]. A similar pattern was found in Geospiza Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology [8], and hybrid Heliconius butterflies preferred the hybrid wing patterning over that of both parent species [12]. Intrinsic differences in habitat use [59] or in phenology [60] may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in Rhagoletis pomonella maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple [61,62] and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In Xiphophorus swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [63]. Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on Helianthus sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences [47,64], in combination with hybridization induced structural differences [47]. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow Passer italiae and its parent species [28]. Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species[65], the population size of the hybrid species[66], the nature of selection acting on hybrids, and linkage among incompatibilities to each other and to adaptive variants [67]. Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive phenotypes [59], or through novel combinations of ecological traits from the parent species [68], and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. ===Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [69] as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization»[45]. Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids [70]. The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [70]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid Helianthus sunflower species genomes [71], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [45]. In Zymoseptoria fungi genomes were stabilized within ca. 400 generations [72], whereas in hybrid Xiphophorus swordtail genomes [73] genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization [74], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [75]. Given time, genetic drift will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations [45]. Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in that hybrids retaining both parental alleles and hence are not homozygous for any weakly deleterious alleles have higher fitness than homozygous hybrids. This associative overdominance [76,77], may slow down the process of fixation of parental alleles through favouring retention of both parental alleles. The effect of assortative overdominance is strongest in low recombination regions, including inversions [78]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [21,79,80]; (Fig.3). An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi [21], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus [81], in Mus domesticus house mice [82], in Heliconius butterflies [80] and in Xiphophorus swordtail fish [43]. Genome-wide incompatibilities have been identified in Xipophorous fish [83], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids [84] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [49,85], fungus [86] and cyto-nuclear incompatibilities in Mimulus plants [87]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [49,84,88] and genes involved in mutagenesis and cancer related pathways [84] may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations [43,73,79]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.|229x229px]] ===Altered genome properties in hybrid taxa=== The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [52,89,90], to activate transposable elements [91-93], and to induce chromosomal rearrangements [94,95]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [96,97]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana [98]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [99]. Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization [100]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [101,102]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [102,103]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained [103]. A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes [104]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [104]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome [102],[105]. Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [105]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [106,107]. Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [108]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [109], potentially buffering against a transcriptomic shock. ===What factors influence the likelihood of the formation of persistent hybrid genomes?=== Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [110]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [111]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [112,113], and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule [114] states that when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [22]. These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [115]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see [116] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [117]. This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes [118], the elevated frequency of loci involved in reproductive isolation [119] and/or the heightened conflict on sex chromosomes [120]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [49] is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer [121][122]. In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae [123] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [123]. For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [124]. Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study [125], and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species [126]. Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis [127], and most if not all asexual vertebrate species are of hybrid origin [128]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [129], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes [130]. In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies[34]. Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes [131]. Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness [132] but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above [131]. An intermediate genetic distance may thus be most condusive to hybrid speciation [131]. Experimental lab crosses support this hypothesis [65]. The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [133]. Relatively equal parental contributions are also found in some homoploid hybrid species [48] but in other cases they are highly unequal such as in some Heliconius species [134]. The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes [135]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [43,44]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance [21] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata [136]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [137]. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries [19,138,139], and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone [140]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. [141]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [45,73]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. [43] or are there generally stable solutions with high contributions from both parent species across the genome c.f. [49]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. [99,133]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana [100]? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ===References=== 1. 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These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [146]. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests [147-149] or f-statistics [150,151]. Modified versions of these tests can be used to infer introgressed genomic regions [152], the direction of gene flow [153,154] or the amount of gene flow [151]. For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited [155-157]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help [158,159]. Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination [156,160-163]. With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [164]. Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [165,166] or with summary statistics in an Approximate Bayesian Computation framework [167]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [168].  ---- ==Glossary== Ancestry block/introgression tracts: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Extrinsic incompatibilities: Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Intrinsic incompatibilities: environment-independent reproductive barriers. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. Phenology: the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: reproductive barrier arising after zygote formation, including inviability and sterility. Post-mating barriers: Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). Pre-mating barriers: Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Prezygotic incompatibilities: reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. Recombination rate: Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinational hybrid speciation: the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. Transgressive phenotypes: extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] =References= <references /> [[Category:PLOS Genetics drafts]] 1. Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, et al. Hybridization and speciation. J Evol Biol. 2013;26: 229–246. doi:10.1111/j.1420-9101.2012.02599.x 2. Fisher RA. The genetical theory of natural selection. Oxford: Clarendon Press; 1930. doi:10.5962/bhl.title.27468 3. Mayr E. Animal Species and Evolution. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 8oqyokiq3nhw6yb6yuwnthkf7fq78xv 7783 7782 2019-06-29T09:22:18Z Annarunemark 132 /* References */ wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is common, and that it may represent an important source of novel variation. Although most interspecific hybrids are sterile or less fit than their parents, some may survive and reproduce, enabling the transfer of adaptive variants across the species boundary, and even result in the formation of novel evolutionary lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel ecological niches, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. The potential for rapid adapation or speciation makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how introgressed alleles or hybrid species can establish and how the resulting hybrid genomes evolve. ==Background== Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour [2] which can result in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals [1,6,7]. Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species [1]. Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the Geospiza Galapagos finches [8], African cichlid fishes [9], Heliconius butterflies [10-12] and Hawaiian Madiinae tarweeds and silverswords [13]. Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species [14,15]. This could potentially lead to reinforcement, selection to strengthen premating isolation [16] or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort [14]. If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [17,18]; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [19]. If hybrids are fertile, hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable neutral or selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occasional gene flow [20,21]. Hybrid fitness may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including Drosophila [22], birds [23] and fish [24]. Hybrid fitness may also differ with cross direction [25], between first generation and later generation hybrids [26], and among individuals within generations of the same cross-type [27,28] . In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [29,30]. Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3 Potential outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial [1]. Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced [31,32], or the adaptive loci are tightly linked to deleterious ones [33]. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from Anopheles gambiae to A. coluzzii [21] and the red warning wing colouration trait in Heliconius butterflies that is under natural selection from predators which has been introgressed from e.g. H. melpomene to H. timareta [34] and other Heliconius species [20]. In the plant Arabidopsis arenosa some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from A. lyrata [35]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [36]. If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolatated against other populations of the same species. Examples of this include Heliconius butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g. [37]), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between H. t. florencia and H. t. linaresi) and intermediate levels (e.g. H. c. galanthus/H. pachinus) of divergence [38]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation [1,29]. A hybrid species has an admixed genome and forms stable genetically distinct populations [29]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation [39], but see [40]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. Heliconius heurippa [10-12], Passer italiae [28], and three Helianthus sunflower species [41] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [39]. Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. [42]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation, [29]). A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exist both between taxa and within lineages of hybrid taxa, see e.g. [43,44]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [40,41,45-49]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an allopolyploid with increased ploidy compared to their parental taxa (Fig. 2). ). In contrast to allopolyploids, autopolyploids are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals [50]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [50]. [[File:Figure2 Homoploid and allopolyploid hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] ===Reproductive isolation against parent species=== Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species [1,39,51]. Reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental condictions (extrinsic or intrinsic barriers, respectively) [52] . For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments [30]. Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier [53-56]. Strong extrinsic pre-zygotic have been shown to isolate the hybrid species Senecio eboracensis from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments [57]. Lowe & Abbott [57] conclude that selfing, timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation. Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [58]. A similar pattern was found in Geospiza Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology [8], and hybrid Heliconius butterflies preferred the hybrid wing patterning over that of both parent species [12]. Intrinsic differences in habitat use [59] or in phenology [60] may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in Rhagoletis pomonella maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple [61,62] and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In Xiphophorus swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [63]. Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on Helianthus sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences [47,64], in combination with hybridization induced structural differences [47]. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow Passer italiae and its parent species [28]. Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species[65], the population size of the hybrid species[66], the nature of selection acting on hybrids, and linkage among incompatibilities to each other and to adaptive variants [67]. Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive phenotypes [59], or through novel combinations of ecological traits from the parent species [68], and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. ===Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [69] as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization»[45]. Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids [70]. The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [70]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid Helianthus sunflower species genomes [71], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [45]. In Zymoseptoria fungi genomes were stabilized within ca. 400 generations [72], whereas in hybrid Xiphophorus swordtail genomes [73] genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization [74], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [75]. Given time, genetic drift will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations [45]. Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in that hybrids retaining both parental alleles and hence are not homozygous for any weakly deleterious alleles have higher fitness than homozygous hybrids. This associative overdominance [76,77], may slow down the process of fixation of parental alleles through favouring retention of both parental alleles. The effect of assortative overdominance is strongest in low recombination regions, including inversions [78]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [21,79,80]; (Fig.3). An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi [21], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus [81], in Mus domesticus house mice [82], in Heliconius butterflies [80] and in Xiphophorus swordtail fish [43]. Genome-wide incompatibilities have been identified in Xipophorous fish [83], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids [84] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [49,85], fungus [86] and cyto-nuclear incompatibilities in Mimulus plants [87]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [49,84,88] and genes involved in mutagenesis and cancer related pathways [84] may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations [43,73,79]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.|229x229px]] ===Altered genome properties in hybrid taxa=== The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [52,89,90], to activate transposable elements [91-93], and to induce chromosomal rearrangements [94,95]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [96,97]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana [98]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [99]. Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization [100]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [101,102]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [102,103]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained [103]. A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes [104]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [104]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome [102],[105]. Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [105]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [106,107]. Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [108]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [109], potentially buffering against a transcriptomic shock. ===What factors influence the likelihood of the formation of persistent hybrid genomes?=== Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [110]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [111]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [112,113], and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule [114] states that when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [22]. These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [115]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see [116] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [117]. This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes [118], the elevated frequency of loci involved in reproductive isolation [119] and/or the heightened conflict on sex chromosomes [120]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [49] is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer [121][122]. In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae [123] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [123]. For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [124]. Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study [125], and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species [126]. Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis [127], and most if not all asexual vertebrate species are of hybrid origin [128]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [129], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes [130]. In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies[34]. Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes [131]. Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness [132] but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above [131]. An intermediate genetic distance may thus be most condusive to hybrid speciation [131]. Experimental lab crosses support this hypothesis [65]. The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [133]. Relatively equal parental contributions are also found in some homoploid hybrid species [48] but in other cases they are highly unequal such as in some Heliconius species [134]. The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes [135]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [43,44]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance [21] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata [136]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [137]. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries [19,138,139], and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone [140]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. [141]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [45,73]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. [43] or are there generally stable solutions with high contributions from both parent species across the genome c.f. [49]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. [99,133]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana [100]? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ===References=== 1. 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These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [146]. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests [147-149] or f-statistics [150,151]. Modified versions of these tests can be used to infer introgressed genomic regions [152], the direction of gene flow [153,154] or the amount of gene flow [151]. For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited [155-157]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help [158,159]. Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination [156,160-163]. With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [164]. Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [165,166] or with summary statistics in an Approximate Bayesian Computation framework [167]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [168].  ---- ==Glossary== Ancestry block/introgression tracts: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Extrinsic incompatibilities: Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Intrinsic incompatibilities: environment-independent reproductive barriers. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. Phenology: the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: reproductive barrier arising after zygote formation, including inviability and sterility. Post-mating barriers: Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). Pre-mating barriers: Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Prezygotic incompatibilities: reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. Recombination rate: Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinational hybrid speciation: the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. Transgressive phenotypes: extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] =References= <references /> [[Category:PLOS Genetics drafts]] References 1. Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, et al. Hybridization and speciation. J Evol Biol. 2013;26: 229–246. doi:10.1111/j.1420-9101.2012.02599.x 2. Fisher RA. The genetical theory of natural selection. Oxford: Clarendon Press; 1930. doi:10.5962/bhl.title.27468 3. Mayr E. Animal Species and Evolution. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 ajzgcndxf816yz0o1e0ld3gm60ivxml 7784 7783 2019-06-29T09:22:43Z Annarunemark 132 /* References */ wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is common, and that it may represent an important source of novel variation. Although most interspecific hybrids are sterile or less fit than their parents, some may survive and reproduce, enabling the transfer of adaptive variants across the species boundary, and even result in the formation of novel evolutionary lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel ecological niches, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. The potential for rapid adapation or speciation makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how introgressed alleles or hybrid species can establish and how the resulting hybrid genomes evolve. ==Background== Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour [2] which can result in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals [1,6,7]. Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species [1]. Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the Geospiza Galapagos finches [8], African cichlid fishes [9], Heliconius butterflies [10-12] and Hawaiian Madiinae tarweeds and silverswords [13]. Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species [14,15]. This could potentially lead to reinforcement, selection to strengthen premating isolation [16] or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort [14]. If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [17,18]; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [19]. If hybrids are fertile, hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable neutral or selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occasional gene flow [20,21]. Hybrid fitness may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including Drosophila [22], birds [23] and fish [24]. Hybrid fitness may also differ with cross direction [25], between first generation and later generation hybrids [26], and among individuals within generations of the same cross-type [27,28] . In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [29,30]. Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3 Potential outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial [1]. Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced [31,32], or the adaptive loci are tightly linked to deleterious ones [33]. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from Anopheles gambiae to A. coluzzii [21] and the red warning wing colouration trait in Heliconius butterflies that is under natural selection from predators which has been introgressed from e.g. H. melpomene to H. timareta [34] and other Heliconius species [20]. In the plant Arabidopsis arenosa some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from A. lyrata [35]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [36]. If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolatated against other populations of the same species. Examples of this include Heliconius butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g. [37]), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between H. t. florencia and H. t. linaresi) and intermediate levels (e.g. H. c. galanthus/H. pachinus) of divergence [38]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation [1,29]. A hybrid species has an admixed genome and forms stable genetically distinct populations [29]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation [39], but see [40]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. Heliconius heurippa [10-12], Passer italiae [28], and three Helianthus sunflower species [41] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [39]. Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. [42]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation, [29]). A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exist both between taxa and within lineages of hybrid taxa, see e.g. [43,44]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [40,41,45-49]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an allopolyploid with increased ploidy compared to their parental taxa (Fig. 2). ). In contrast to allopolyploids, autopolyploids are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals [50]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [50]. [[File:Figure2 Homoploid and allopolyploid hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] ===Reproductive isolation against parent species=== Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species [1,39,51]. Reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental condictions (extrinsic or intrinsic barriers, respectively) [52] . For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments [30]. Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier [53-56]. Strong extrinsic pre-zygotic have been shown to isolate the hybrid species Senecio eboracensis from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments [57]. Lowe & Abbott [57] conclude that selfing, timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation. Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [58]. A similar pattern was found in Geospiza Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology [8], and hybrid Heliconius butterflies preferred the hybrid wing patterning over that of both parent species [12]. Intrinsic differences in habitat use [59] or in phenology [60] may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in Rhagoletis pomonella maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple [61,62] and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In Xiphophorus swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [63]. Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on Helianthus sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences [47,64], in combination with hybridization induced structural differences [47]. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow Passer italiae and its parent species [28]. Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species[65], the population size of the hybrid species[66], the nature of selection acting on hybrids, and linkage among incompatibilities to each other and to adaptive variants [67]. Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive phenotypes [59], or through novel combinations of ecological traits from the parent species [68], and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. ===Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [69] as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization»[45]. Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids [70]. The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [70]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid Helianthus sunflower species genomes [71], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [45]. In Zymoseptoria fungi genomes were stabilized within ca. 400 generations [72], whereas in hybrid Xiphophorus swordtail genomes [73] genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization [74], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [75]. Given time, genetic drift will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations [45]. Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in that hybrids retaining both parental alleles and hence are not homozygous for any weakly deleterious alleles have higher fitness than homozygous hybrids. This associative overdominance [76,77], may slow down the process of fixation of parental alleles through favouring retention of both parental alleles. The effect of assortative overdominance is strongest in low recombination regions, including inversions [78]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [21,79,80]; (Fig.3). An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi [21], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus [81], in Mus domesticus house mice [82], in Heliconius butterflies [80] and in Xiphophorus swordtail fish [43]. Genome-wide incompatibilities have been identified in Xipophorous fish [83], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids [84] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [49,85], fungus [86] and cyto-nuclear incompatibilities in Mimulus plants [87]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [49,84,88] and genes involved in mutagenesis and cancer related pathways [84] may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations [43,73,79]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.|229x229px]] ===Altered genome properties in hybrid taxa=== The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [52,89,90], to activate transposable elements [91-93], and to induce chromosomal rearrangements [94,95]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [96,97]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana [98]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [99]. Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization [100]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [101,102]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [102,103]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained [103]. A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes [104]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [104]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome [102],[105]. Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [105]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [106,107]. Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [108]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [109], potentially buffering against a transcriptomic shock. ===What factors influence the likelihood of the formation of persistent hybrid genomes?=== Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [110]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [111]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [112,113], and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule [114] states that when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [22]. These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [115]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see [116] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [117]. This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes [118], the elevated frequency of loci involved in reproductive isolation [119] and/or the heightened conflict on sex chromosomes [120]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [49] is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer [121][122]. In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae [123] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [123]. For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [124]. Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study [125], and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species [126]. Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis [127], and most if not all asexual vertebrate species are of hybrid origin [128]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [129], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes [130]. In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies[34]. Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes [131]. Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness [132] but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above [131]. An intermediate genetic distance may thus be most condusive to hybrid speciation [131]. Experimental lab crosses support this hypothesis [65]. The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [133]. Relatively equal parental contributions are also found in some homoploid hybrid species [48] but in other cases they are highly unequal such as in some Heliconius species [134]. The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes [135]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [43,44]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance [21] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata [136]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [137]. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries [19,138,139], and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone [140]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. [141]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [45,73]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. [43] or are there generally stable solutions with high contributions from both parent species across the genome c.f. [49]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. [99,133]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana [100]? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ==Box: Detecting and studying hybridization with genomic tools== Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE [143], ADMIXTURE [144] or fineSTRUCTURE [145]. These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [146]. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests [147-149] or f-statistics [150,151]. Modified versions of these tests can be used to infer introgressed genomic regions [152], the direction of gene flow [153,154] or the amount of gene flow [151]. For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited [155-157]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help [158,159]. Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination [156,160-163]. With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [164]. Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [165,166] or with summary statistics in an Approximate Bayesian Computation framework [167]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [168].  ---- ==Glossary== Ancestry block/introgression tracts: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Extrinsic incompatibilities: Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Intrinsic incompatibilities: environment-independent reproductive barriers. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. Phenology: the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: reproductive barrier arising after zygote formation, including inviability and sterility. Post-mating barriers: Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). Pre-mating barriers: Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Prezygotic incompatibilities: reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. Recombination rate: Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinational hybrid speciation: the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. Transgressive phenotypes: extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] =References= <references /> [[Category:PLOS Genetics drafts]] References 1. Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, et al. Hybridization and speciation. J Evol Biol. 2013;26: 229–246. doi:10.1111/j.1420-9101.2012.02599.x 2. Fisher RA. The genetical theory of natural selection. Oxford: Clarendon Press; 1930. doi:10.5962/bhl.title.27468 3. Mayr E. Animal Species and Evolution. Cambridge, MA and London, England: Harvard University Press; 1963. doi:10.4159/harvard.9780674865327 4. Stebbins GL. The Role of Hybridization in Evolution. Proc. Am. Philos. Soc. 1959;103: 231–251. 5. Andersson E, Stebbins GL. Hybridization as an evolutionary stimulus. Evolution. 1954;4: 378–388. 6. Arnold ML. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 28mpkjqxeibd94eixwei5ghiki5gs1h 7796 7784 2019-07-04T06:40:12Z T Shafee 80 /* Abstract */ + hyperlinks as examples wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and [[w:homoploid:homoploid]], which are a [[w:Mosaic (genetics)|mosaic]] of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. ==Background== Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour [2] which can result in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals [1,6,7]. Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species [1]. Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the Geospiza Galapagos finches [8], African cichlid fishes [9], Heliconius butterflies [10-12] and Hawaiian Madiinae tarweeds and silverswords [13]. Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species [14,15]. This could potentially lead to reinforcement, selection to strengthen premating isolation [16] or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort [14]. If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [17,18]; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [19]. If hybrids are fertile, hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable neutral or selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occasional gene flow [20,21]. Hybrid fitness may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including Drosophila [22], birds [23] and fish [24]. Hybrid fitness may also differ with cross direction [25], between first generation and later generation hybrids [26], and among individuals within generations of the same cross-type [27,28] . In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [29,30]. Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3 Potential outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial [1]. Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced [31,32], or the adaptive loci are tightly linked to deleterious ones [33]. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from Anopheles gambiae to A. coluzzii [21] and the red warning wing colouration trait in Heliconius butterflies that is under natural selection from predators which has been introgressed from e.g. H. melpomene to H. timareta [34] and other Heliconius species [20]. In the plant Arabidopsis arenosa some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from A. lyrata [35]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [36]. If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolatated against other populations of the same species. Examples of this include Heliconius butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g. [37]), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between H. t. florencia and H. t. linaresi) and intermediate levels (e.g. H. c. galanthus/H. pachinus) of divergence [38]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation [1,29]. A hybrid species has an admixed genome and forms stable genetically distinct populations [29]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation [39], but see [40]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. Heliconius heurippa [10-12], Passer italiae [28], and three Helianthus sunflower species [41] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [39]. Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. [42]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation, [29]). A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exist both between taxa and within lineages of hybrid taxa, see e.g. [43,44]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [40,41,45-49]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an allopolyploid with increased ploidy compared to their parental taxa (Fig. 2). ). In contrast to allopolyploids, autopolyploids are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals [50]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [50]. [[File:Figure2 Homoploid and allopolyploid hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] ===Reproductive isolation against parent species=== Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species [1,39,51]. Reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental condictions (extrinsic or intrinsic barriers, respectively) [52] . For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments [30]. Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier [53-56]. Strong extrinsic pre-zygotic have been shown to isolate the hybrid species Senecio eboracensis from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments [57]. Lowe & Abbott [57] conclude that selfing, timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation. Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [58]. A similar pattern was found in Geospiza Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology [8], and hybrid Heliconius butterflies preferred the hybrid wing patterning over that of both parent species [12]. Intrinsic differences in habitat use [59] or in phenology [60] may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in Rhagoletis pomonella maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple [61,62] and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In Xiphophorus swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [63]. Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on Helianthus sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences [47,64], in combination with hybridization induced structural differences [47]. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow Passer italiae and its parent species [28]. Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species[65], the population size of the hybrid species[66], the nature of selection acting on hybrids, and linkage among incompatibilities to each other and to adaptive variants [67]. Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive phenotypes [59], or through novel combinations of ecological traits from the parent species [68], and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. ===Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [69] as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization»[45]. Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids [70]. The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [70]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid Helianthus sunflower species genomes [71], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [45]. In Zymoseptoria fungi genomes were stabilized within ca. 400 generations [72], whereas in hybrid Xiphophorus swordtail genomes [73] genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization [74], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [75]. Given time, genetic drift will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations [45]. Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in that hybrids retaining both parental alleles and hence are not homozygous for any weakly deleterious alleles have higher fitness than homozygous hybrids. This associative overdominance [76,77], may slow down the process of fixation of parental alleles through favouring retention of both parental alleles. The effect of assortative overdominance is strongest in low recombination regions, including inversions [78]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [21,79,80]; (Fig.3). An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi [21], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus [81], in Mus domesticus house mice [82], in Heliconius butterflies [80] and in Xiphophorus swordtail fish [43]. Genome-wide incompatibilities have been identified in Xipophorous fish [83], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids [84] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [49,85], fungus [86] and cyto-nuclear incompatibilities in Mimulus plants [87]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [49,84,88] and genes involved in mutagenesis and cancer related pathways [84] may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations [43,73,79]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.|229x229px]] ===Altered genome properties in hybrid taxa=== The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [52,89,90], to activate transposable elements [91-93], and to induce chromosomal rearrangements [94,95]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [96,97]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana [98]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [99]. Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization [100]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [101,102]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [102,103]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained [103]. A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes [104]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [104]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome [102],[105]. Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [105]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [106,107]. Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [108]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [109], potentially buffering against a transcriptomic shock. ===What factors influence the likelihood of the formation of persistent hybrid genomes?=== Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [110]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [111]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [112,113], and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule [114] states that when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [22]. These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [115]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see [116] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [117]. This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes [118], the elevated frequency of loci involved in reproductive isolation [119] and/or the heightened conflict on sex chromosomes [120]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [49] is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer [121][122]. In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae [123] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [123]. For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [124]. Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study [125], and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species [126]. Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis [127], and most if not all asexual vertebrate species are of hybrid origin [128]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [129], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes [130]. In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies[34]. Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes [131]. Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness [132] but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above [131]. An intermediate genetic distance may thus be most condusive to hybrid speciation [131]. Experimental lab crosses support this hypothesis [65]. The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [133]. Relatively equal parental contributions are also found in some homoploid hybrid species [48] but in other cases they are highly unequal such as in some Heliconius species [134]. The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes [135]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [43,44]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance [21] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata [136]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [137]. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries [19,138,139], and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone [140]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. [141]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [45,73]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. [43] or are there generally stable solutions with high contributions from both parent species across the genome c.f. [49]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. [99,133]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana [100]? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ==Box: Detecting and studying hybridization with genomic tools== Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE [143], ADMIXTURE [144] or fineSTRUCTURE [145]. These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [146]. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests [147-149] or f-statistics [150,151]. Modified versions of these tests can be used to infer introgressed genomic regions [152], the direction of gene flow [153,154] or the amount of gene flow [151]. For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited [155-157]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help [158,159]. Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination [156,160-163]. With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [164]. Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [165,166] or with summary statistics in an Approximate Bayesian Computation framework [167]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [168].  ---- ==Glossary== Ancestry block/introgression tracts: a region in the genome of a hybrid where all alleles are inherited from the same parent species. Allopolyploid species: a polyploid hybrid species where the two chromosome sets are derived from different parent species. Backcrossing: crossing of a hybrid with one of its parent species. Extrinsic incompatibilities: Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. Genome stabilization: the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. Hybrid: offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. Hybrid genome: The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. Hybrid zone: geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. Homoploid hybridization: the formation of a hybrid with no change in chromosome number. Incomplete lineage sorting: when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. Introgressive hybridization: hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. Intrinsic incompatibilities: environment-independent reproductive barriers. Linkage disequilibrium: the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. Phenology: the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. Polyploid hybridization: the formation of a hybrid involving whole genome duplication. Postzygotic incompatibilities: reproductive barrier arising after zygote formation, including inviability and sterility. Post-mating barriers: Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). Pre-mating barriers: Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. Prezygotic incompatibilities: reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. Reproductive isolation: the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. Recombination rate: Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. Recombinational hybrid speciation: the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 ini814ek4q1oc3pwdp62uvlyhgruopj 7895 7796 2019-07-23T07:21:05Z T Shafee 80 /* Glossary */ format glossary per [[w:Template:Glossary_infobox]] wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and [[w:homoploid:homoploid]], which are a [[w:Mosaic (genetics)|mosaic]] of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. ==Background== Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion [1]. Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour [2] which can result in breaking up co-adapted gene complexes [3]. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity [4,5]. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals [1,6,7]. Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species [1]. Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the Geospiza Galapagos finches [8], African cichlid fishes [9], Heliconius butterflies [10-12] and Hawaiian Madiinae tarweeds and silverswords [13]. Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). ===Evolutionary outcomes of hybridization=== There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species [14,15]. This could potentially lead to reinforcement, selection to strengthen premating isolation [16] or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort [14]. If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal, [17,18]; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa [19]. If hybrids are fertile, hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable neutral or selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occasional gene flow [20,21]. Hybrid fitness may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including Drosophila [22], birds [23] and fish [24]. Hybrid fitness may also differ with cross direction [25], between first generation and later generation hybrids [26], and among individuals within generations of the same cross-type [27,28] . In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa [29,30]. Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3 Potential outcomes of hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] ===Adaptive introgression=== When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial [1]. Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced [31,32], or the adaptive loci are tightly linked to deleterious ones [33]. Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from Anopheles gambiae to A. coluzzii [21] and the red warning wing colouration trait in Heliconius butterflies that is under natural selection from predators which has been introgressed from e.g. H. melpomene to H. timareta [34] and other Heliconius species [20]. In the plant Arabidopsis arenosa some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from A. lyrata [35]. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans [36]. If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolatated against other populations of the same species. Examples of this include Heliconius butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g. [37]), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between H. t. florencia and H. t. linaresi) and intermediate levels (e.g. H. c. galanthus/H. pachinus) of divergence [38]. ===What is a hybrid species?=== One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation [1,29]. A hybrid species has an admixed genome and forms stable genetically distinct populations [29]. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation [39], but see [40]. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. Heliconius heurippa [10-12], Passer italiae [28], and three Helianthus sunflower species [41] because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown [39]. Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. [42]). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation, [29]). A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exist both between taxa and within lineages of hybrid taxa, see e.g. [43,44]. ===Homoploid and polyploid hybrid speciation=== In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2) [1]. The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination [40,41,45-49]. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an allopolyploid with increased ploidy compared to their parental taxa (Fig. 2). ). In contrast to allopolyploids, autopolyploids are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals [50]. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences [50]. [[File:Figure2 Homoploid and allopolyploid hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] ===Reproductive isolation against parent species=== Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species [1,39,51]. Reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental condictions (extrinsic or intrinsic barriers, respectively) [52] . For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments [30]. Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier [53-56]. Strong extrinsic pre-zygotic have been shown to isolate the hybrid species Senecio eboracensis from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments [57]. Lowe & Abbott [57] conclude that selfing, timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation. Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids [58]. A similar pattern was found in Geospiza Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology [8], and hybrid Heliconius butterflies preferred the hybrid wing patterning over that of both parent species [12]. Intrinsic differences in habitat use [59] or in phenology [60] may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in Rhagoletis pomonella maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple [61,62] and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In Xiphophorus swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions [63]. Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on Helianthus sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences [47,64], in combination with hybridization induced structural differences [47]. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow Passer italiae and its parent species [28]. Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species[65], the population size of the hybrid species[66], the nature of selection acting on hybrids, and linkage among incompatibilities to each other and to adaptive variants [67]. Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive phenotypes [59], or through novel combinations of ecological traits from the parent species [68], and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. ===Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits [69] as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as «genome stabilization»[45]. Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids [70]. The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome [70]. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid Helianthus sunflower species genomes [71], and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations [45]. In Zymoseptoria fungi genomes were stabilized within ca. 400 generations [72], whereas in hybrid Xiphophorus swordtail genomes [73] genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization [74], and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event [75]. Given time, genetic drift will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations [45]. Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in that hybrids retaining both parental alleles and hence are not homozygous for any weakly deleterious alleles have higher fitness than homozygous hybrids. This associative overdominance [76,77], may slow down the process of fixation of parental alleles through favouring retention of both parental alleles. The effect of assortative overdominance is strongest in low recombination regions, including inversions [78]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization [21,79,80]; (Fig.3). An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi [21], suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus [81], in Mus domesticus house mice [82], in Heliconius butterflies [80] and in Xiphophorus swordtail fish [43]. Genome-wide incompatibilities have been identified in Xipophorous fish [83], chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids [84] and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows [49,85], fungus [86] and cyto-nuclear incompatibilities in Mimulus plants [87]. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair [49,84,88] and genes involved in mutagenesis and cancer related pathways [84] may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations [43,73,79]. [[File:Figure3 Hybrid genome stabilization.jpg|thumb|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.|229x229px]] ===Altered genome properties in hybrid taxa=== The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates [52,89,90], to activate transposable elements [91-93], and to induce chromosomal rearrangements [94,95]. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption [96,97]. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana [98]. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease [99]. Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization [100]. Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid [101,102]. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes [102,103]. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained [103]. A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes [104]. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent [104]. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome [102],[105]. Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers [105]. In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species [106,107]. Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations [108]. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability [109], potentially buffering against a transcriptomic shock. ===What factors influence the likelihood of the formation of persistent hybrid genomes?=== Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species [110]. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes [111]. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation [112,113], and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule [114] states that when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids [22]. These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression [115]. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see [116] for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems [117]. This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes [118], the elevated frequency of loci involved in reproductive isolation [119] and/or the heightened conflict on sex chromosomes [120]. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows [49] is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades [4]. In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer [121][122]. In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae [123] in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells [123]. For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating [124]. Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study [125], and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species [126]. Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis [127], and most if not all asexual vertebrate species are of hybrid origin [128]. Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants [129], suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes [130]. In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies[34]. Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. ===What genes and genomic regions are affected by hybridization?=== Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes [131]. Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness [132] but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above [131]. An intermediate genetic distance may thus be most condusive to hybrid speciation [131]. Experimental lab crosses support this hypothesis [65]. The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome [133]. Relatively equal parental contributions are also found in some homoploid hybrid species [48] but in other cases they are highly unequal such as in some Heliconius species [134]. The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes [135]. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited [43,44]. Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance [21] and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata [136]. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci [137]. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries [19,138,139], and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone [140]. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. [141]. ===Conclusions and future directions=== Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization [45,73]? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. [43] or are there generally stable solutions with high contributions from both parent species across the genome c.f. [49]? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. [99,133]? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana [100]? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. ==Box: Detecting and studying hybridization with genomic tools== Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE [143], ADMIXTURE [144] or fineSTRUCTURE [145]. These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization [146]. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests [147-149] or f-statistics [150,151]. Modified versions of these tests can be used to infer introgressed genomic regions [152], the direction of gene flow [153,154] or the amount of gene flow [151]. For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited [155-157]. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help [158,159]. Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination [156,160-163]. With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa [164]. Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum [165,166] or with summary statistics in an Approximate Bayesian Computation framework [167]. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum [168].  ---- ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] =References= <references /> [[Category:PLOS Genetics drafts]] References 1. Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, et al. Hybridization and speciation. J Evol Biol. 2013;26: 229–246. doi:10.1111/j.1420-9101.2012.02599.x 2. Fisher RA. 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Evol. 2017;9: 427–437. doi:10.1093/gbe/evx018 9ihzptgbf0bdv2bmpjbayos4b5mebyd 7919 7895 2019-07-28T05:46:31Z T Shafee 80 reference formatting wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and [[w:homoploid:homoploid]], which are a [[w:Mosaic (genetics)|mosaic]] of the parent species with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted gene complexes.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the Geospiza Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> Heliconius butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian Madiinae tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to reinforcement, selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable neutral or selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occasional gene flow.<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid fitness may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including Drosophila,<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" /> Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive loci are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from Anopheles gambiae to A. coluzzii<ref name=":20" /> and the red warning wing colouration trait in Heliconius butterflies that is under natural selection from predators which has been introgressed from e.g. H. melpomene to H. timareta<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other Heliconius species.<ref name=":19" /> In the plant Arabidopsis arenosa some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from A. lyrata.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolatated against other populations of the same species. Examples of this include Heliconius butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between H. t. florencia and H. t. linaresi) and intermediate levels (e.g. H. c. galanthus/H. pachinus) of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. Heliconius heurippa,<ref name=":9" /><ref name=":10" /><ref name=":11" /> asser italiae,<ref name=":27" /> and three Helianthus sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exist both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination.<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an allopolyploid with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, autopolyploids are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences.<ref name=":49" /> [[File:Figure2_Homoploid_and_allopolyploid_hybridization.svg|link=Special:FilePath/Figure2_Homoploid_and_allopolyploid_hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental condictions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic have been shown to isolate the hybrid species Senecio eboracensis from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that selfing, timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in Geospiza Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid Heliconius butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in Rhagoletis pomonella maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In Xiphophorus swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on Helianthus sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow Passer italiae and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and linkage among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation. Hybrid species have been shown to adapt to novel ecological niches through transgressive phenotypes,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome.<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid Helianthus sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In Zymoseptoria fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid Xiphophorus swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, genetic drift will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in that hybrids retaining both parental alleles and hence are not homozygous for any weakly deleterious alleles have higher fitness than homozygous hybrids. This associative overdominance,<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental alleles. The effect of assortative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi,<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus,<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in Mus domesticus house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in Heliconius butterflies<ref name=":79" /> and in Xiphophorus swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in Xipophorous fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in Mimulus plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure3_Hybrid_genome_stabilization.jpg|thumb|229x229px|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce chromosomal rearrangements.<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis,<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, artic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some Heliconius species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. F.|date=2009|editor-last=Nachman|editor-first=Michael W.|title=The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing|url=https://dx.plos.org/10.1371/journal.pgen.1000550|journal=PLoS Genetics|language=en|volume=5|issue=7|pages=e1000550|doi=10.1371/journal.pgen.1000550|issn=1553-7404|pmc=PMC2696600|pmid=19578407}}</ref><ref name=":147">{{Citation|last=Green|first=R. E.|last2=Krause|first2=J.|last3=Briggs|first3=A. W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> fqrzhvlmiou0azk08ezg4t87ur07afa 8070 7919 2019-08-12T10:54:16Z Annarunemark 132 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adapations or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted gene complexes.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the Geospiza Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> Heliconius butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian Madiinae tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to reinforcement, selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable neutral or selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occasional gene flow.<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid fitness may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including Drosophila,<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive loci are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from Anopheles gambiae to A. coluzzii<ref name=":20" /> and the red warning wing colouration trait in Heliconius butterflies that is under natural selection from predators which has been introgressed from e.g. H. melpomene to H. timareta<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other Heliconius species.<ref name=":19" /> In the plant Arabidopsis arenosa some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from A. lyrata.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolatated against other populations of the same species. Examples of this include Heliconius butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between H. t. florencia and H. t. linaresi) and intermediate levels (e.g. H. c. galanthus/H. pachinus) of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. Heliconius heurippa,<ref name=":9" /><ref name=":10" /><ref name=":11" /> asser italiae,<ref name=":27" /> and three Helianthus sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination.<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an allopolyploid with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, autopolyploids are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences.<ref name=":49" /> [[File:Figure2_Homoploid_and_allopolyploid_hybridization.svg|link=Special:FilePath/Figure2_Homoploid_and_allopolyploid_hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental condictions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic have been shown to isolate the hybrid species Senecio eboracensis from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that selfing, timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in Geospiza Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid Heliconius butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in Rhagoletis pomonella maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In Xiphophorus swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on Helianthus sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow Passer italiae and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and linkage among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through transgressive phenotypes,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome.<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid Helianthus sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In Zymoseptoria fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid Xiphophorus swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, genetic drift will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not homozygous for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative overdominance,<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi,<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus,<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in Mus domesticus house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in Heliconius butterflies<ref name=":79" /> and in Xiphophorus swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in Xipophorous fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in Mimulus plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure3_Hybrid_genome_stabilization.jpg|thumb|229x229px|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce chromosomal rearrangements.<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis,<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some Heliconius species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. F.|date=2009|editor-last=Nachman|editor-first=Michael W.|title=The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing|url=https://dx.plos.org/10.1371/journal.pgen.1000550|journal=PLoS Genetics|language=en|volume=5|issue=7|pages=e1000550|doi=10.1371/journal.pgen.1000550|issn=1553-7404|pmc=PMC2696600|pmid=19578407}}</ref><ref name=":147">{{Citation|last=Green|first=R. E.|last2=Krause|first2=J.|last3=Briggs|first3=A. W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> lyczjqlwmbo3iqzyzoar95hm1g4yyq4 8071 8070 2019-08-12T12:30:53Z Annarunemark 132 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic [[w:adaptation|adaptation]]s or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted gene complexes.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the Geospiza Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> Heliconius butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian Madiinae tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to reinforcement, selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable neutral or selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occasional gene flow.<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid fitness may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including Drosophila,<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive loci are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from Anopheles gambiae to A. coluzzii<ref name=":20" /> and the red warning wing colouration trait in Heliconius butterflies that is under natural selection from predators which has been introgressed from e.g. H. melpomene to H. timareta<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other Heliconius species.<ref name=":19" /> In the plant Arabidopsis arenosa some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from A. lyrata.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolatated against other populations of the same species. Examples of this include Heliconius butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between H. t. florencia and H. t. linaresi) and intermediate levels (e.g. H. c. galanthus/H. pachinus) of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. Heliconius heurippa,<ref name=":9" /><ref name=":10" /><ref name=":11" /> asser italiae,<ref name=":27" /> and three Helianthus sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination.<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an allopolyploid with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, autopolyploids are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences.<ref name=":49" /> [[File:Figure2_Homoploid_and_allopolyploid_hybridization.svg|link=Special:FilePath/Figure2_Homoploid_and_allopolyploid_hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental condictions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic have been shown to isolate the hybrid species Senecio eboracensis from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that selfing, timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in Geospiza Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid Heliconius butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in Rhagoletis pomonella maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In Xiphophorus swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on Helianthus sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow Passer italiae and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and linkage among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through transgressive phenotypes,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome.<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid Helianthus sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In Zymoseptoria fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid Xiphophorus swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, genetic drift will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not homozygous for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative overdominance,<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi,<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus,<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in Mus domesticus house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in Heliconius butterflies<ref name=":79" /> and in Xiphophorus swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in Xipophorous fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in Mimulus plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure3_Hybrid_genome_stabilization.jpg|thumb|229x229px|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce chromosomal rearrangements.<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis,<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some Heliconius species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. F.|date=2009|editor-last=Nachman|editor-first=Michael W.|title=The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing|url=https://dx.plos.org/10.1371/journal.pgen.1000550|journal=PLoS Genetics|language=en|volume=5|issue=7|pages=e1000550|doi=10.1371/journal.pgen.1000550|issn=1553-7404|pmc=PMC2696600|pmid=19578407}}</ref><ref name=":147">{{Citation|last=Green|first=R. E.|last2=Krause|first2=J.|last3=Briggs|first3=A. W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> f63dznq36bimpu7wj29pdyi88tk77ev 8072 8071 2019-08-12T12:34:33Z Annarunemark 132 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and [[w:Hybridisation_(biology)|hybridization]] between recently diverged species can lead to loss of genetic [[w:adaptation|adaptation]]s or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted [[w:gene complex|supergene]]s.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the Geospiza Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> Heliconius butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian Madiinae tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to reinforcement, selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable neutral or selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occasional gene flow.<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid fitness may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including Drosophila,<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive loci are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from Anopheles gambiae to A. coluzzii<ref name=":20" /> and the red warning wing colouration trait in Heliconius butterflies that is under natural selection from predators which has been introgressed from e.g. H. melpomene to H. timareta<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other Heliconius species.<ref name=":19" /> In the plant Arabidopsis arenosa some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from A. lyrata.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolatated against other populations of the same species. Examples of this include Heliconius butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between H. t. florencia and H. t. linaresi) and intermediate levels (e.g. H. c. galanthus/H. pachinus) of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. Heliconius heurippa,<ref name=":9" /><ref name=":10" /><ref name=":11" /> asser italiae,<ref name=":27" /> and three Helianthus sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination.<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an allopolyploid with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, autopolyploids are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences.<ref name=":49" /> [[File:Figure2_Homoploid_and_allopolyploid_hybridization.svg|link=Special:FilePath/Figure2_Homoploid_and_allopolyploid_hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental condictions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic have been shown to isolate the hybrid species Senecio eboracensis from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that selfing, timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in Geospiza Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid Heliconius butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in Rhagoletis pomonella maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In Xiphophorus swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on Helianthus sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow Passer italiae and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and linkage among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through transgressive phenotypes,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome.<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid Helianthus sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In Zymoseptoria fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid Xiphophorus swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, genetic drift will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not homozygous for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative overdominance,<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi,<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus,<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in Mus domesticus house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in Heliconius butterflies<ref name=":79" /> and in Xiphophorus swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in Xipophorous fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in Mimulus plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure3_Hybrid_genome_stabilization.jpg|thumb|229x229px|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce chromosomal rearrangements.<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis,<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some Heliconius species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. F.|date=2009|editor-last=Nachman|editor-first=Michael W.|title=The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing|url=https://dx.plos.org/10.1371/journal.pgen.1000550|journal=PLoS Genetics|language=en|volume=5|issue=7|pages=e1000550|doi=10.1371/journal.pgen.1000550|issn=1553-7404|pmc=PMC2696600|pmid=19578407}}</ref><ref name=":147">{{Citation|last=Green|first=R. E.|last2=Krause|first2=J.|last3=Briggs|first3=A. W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> 7yjfrg9v8mftrjkz7q5sehqa0wvnq77 8073 8072 2019-08-12T12:35:32Z Annarunemark 132 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and [[w:Hybridisation_(biology)|hybridization]] between recently diverged species can lead to loss of genetic [[w:adaptation|adaptation]]s or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted [[w:supergene|gene complex]]s.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the Geospiza Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> Heliconius butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian Madiinae tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to reinforcement, selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable neutral or selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occasional gene flow.<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid fitness may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including Drosophila,<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive loci are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from Anopheles gambiae to A. coluzzii<ref name=":20" /> and the red warning wing colouration trait in Heliconius butterflies that is under natural selection from predators which has been introgressed from e.g. H. melpomene to H. timareta<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other Heliconius species.<ref name=":19" /> In the plant Arabidopsis arenosa some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from A. lyrata.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolatated against other populations of the same species. Examples of this include Heliconius butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between H. t. florencia and H. t. linaresi) and intermediate levels (e.g. H. c. galanthus/H. pachinus) of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. Heliconius heurippa,<ref name=":9" /><ref name=":10" /><ref name=":11" /> asser italiae,<ref name=":27" /> and three Helianthus sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination.<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an allopolyploid with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, autopolyploids are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences.<ref name=":49" /> [[File:Figure2_Homoploid_and_allopolyploid_hybridization.svg|link=Special:FilePath/Figure2_Homoploid_and_allopolyploid_hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental condictions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic have been shown to isolate the hybrid species Senecio eboracensis from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that selfing, timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in Geospiza Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid Heliconius butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in Rhagoletis pomonella maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In Xiphophorus swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on Helianthus sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow Passer italiae and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and linkage among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through transgressive phenotypes,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome.<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid Helianthus sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In Zymoseptoria fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid Xiphophorus swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, genetic drift will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not homozygous for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative overdominance,<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi,<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus,<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in Mus domesticus house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in Heliconius butterflies<ref name=":79" /> and in Xiphophorus swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in Xipophorous fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in Mimulus plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure3_Hybrid_genome_stabilization.jpg|thumb|229x229px|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce chromosomal rearrangements.<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis,<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some Heliconius species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. F.|date=2009|editor-last=Nachman|editor-first=Michael W.|title=The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing|url=https://dx.plos.org/10.1371/journal.pgen.1000550|journal=PLoS Genetics|language=en|volume=5|issue=7|pages=e1000550|doi=10.1371/journal.pgen.1000550|issn=1553-7404|pmc=PMC2696600|pmid=19578407}}</ref><ref name=":147">{{Citation|last=Green|first=R. E.|last2=Krause|first2=J.|last3=Briggs|first3=A. W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> hqkklqab23sh7atxiv82boz8fp5gdej 8074 8073 2019-08-12T12:39:48Z Annarunemark 132 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and [[w:Hybridisation_(biology)|hybridization]] between recently diverged species can lead to loss of genetic [[w:adaptation|adaptation]]s or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted [[w:supergene|gene complex]]es.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> Heliconius butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian Madiinae tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to reinforcement, selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids backcrossing with parental species. Such introgressive hybridization may enable neutral or selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occasional gene flow.<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid fitness may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including Drosophila,<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive loci are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include a resistance gene that was transferred from Anopheles gambiae to A. coluzzii<ref name=":20" /> and the red warning wing colouration trait in Heliconius butterflies that is under natural selection from predators which has been introgressed from e.g. H. melpomene to H. timareta<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other Heliconius species.<ref name=":19" /> In the plant Arabidopsis arenosa some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from A. lyrata.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolatated against other populations of the same species. Examples of this include Heliconius butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between H. t. florencia and H. t. linaresi) and intermediate levels (e.g. H. c. galanthus/H. pachinus) of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. Heliconius heurippa,<ref name=":9" /><ref name=":10" /><ref name=":11" /> asser italiae,<ref name=":27" /> and three Helianthus sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination.<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an allopolyploid with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, autopolyploids are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences.<ref name=":49" /> [[File:Figure2_Homoploid_and_allopolyploid_hybridization.svg|link=Special:FilePath/Figure2_Homoploid_and_allopolyploid_hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental condictions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic have been shown to isolate the hybrid species Senecio eboracensis from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that selfing, timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in Geospiza Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid Heliconius butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in Rhagoletis pomonella maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In Xiphophorus swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on Helianthus sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow Passer italiae and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and linkage among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through transgressive phenotypes,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome.<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid Helianthus sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In Zymoseptoria fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid Xiphophorus swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, genetic drift will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not homozygous for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative overdominance,<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi,<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus,<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in Mus domesticus house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in Heliconius butterflies<ref name=":79" /> and in Xiphophorus swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in Xipophorous fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in Mimulus plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure3_Hybrid_genome_stabilization.jpg|thumb|229x229px|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce chromosomal rearrangements.<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis,<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some Heliconius species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. F.|date=2009|editor-last=Nachman|editor-first=Michael W.|title=The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing|url=https://dx.plos.org/10.1371/journal.pgen.1000550|journal=PLoS Genetics|language=en|volume=5|issue=7|pages=e1000550|doi=10.1371/journal.pgen.1000550|issn=1553-7404|pmc=PMC2696600|pmid=19578407}}</ref><ref name=":147">{{Citation|last=Green|first=R. E.|last2=Krause|first2=J.|last3=Briggs|first3=A. W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> 1el5vgfuzzoj4iio98r74pdb7byf5am 8075 8074 2019-08-12T12:56:19Z Annarunemark 132 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and [[w:Hybridisation_(biology)|hybridization]] between recently diverged species can lead to loss of genetic [[w:adaptation|adaptation]]s or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted [[w:supergene|gene complex]]es.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> ''Heliconius'' butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian ''Madiinae'' tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to [[w:reinforcement speciation|reinforcement]], selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids [[w:backcrossing|backcrosssing]] with parental species. Such introgressive hybridization may enable neutral or selectively beneficial [[w:allele|allele]]s to be transferred across species boundaries even in species pairs that remain distinct despite occasional [[w:gene flow|gene flow]].<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid [[w:fitness biology|fitness]] may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including ''Drosophila'',<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />)) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive [[w:loci|loci]] are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include an insecticide resistance gene that was transferred from ''Anopheles gambiae'' to ''A. coluzzii''<ref name=":20" /> and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta''<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other ''Heliconius'' species.<ref name=":19" /> In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and [[w:phytotoxicity|phytotoxic]] levels of metal have been introgressed from ''A. lyrata''.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolatated against other populations of the same species. Examples of this include Heliconius butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between H. t. florencia and H. t. linaresi) and intermediate levels (e.g. H. c. galanthus/H. pachinus) of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. Heliconius heurippa,<ref name=":9" /><ref name=":10" /><ref name=":11" /> asser italiae,<ref name=":27" /> and three Helianthus sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination.<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an allopolyploid with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, autopolyploids are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences.<ref name=":49" /> [[File:Figure2_Homoploid_and_allopolyploid_hybridization.svg|link=Special:FilePath/Figure2_Homoploid_and_allopolyploid_hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental condictions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic have been shown to isolate the hybrid species Senecio eboracensis from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that selfing, timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in Geospiza Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid Heliconius butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in Rhagoletis pomonella maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In Xiphophorus swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on Helianthus sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow Passer italiae and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and linkage among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through transgressive phenotypes,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome.<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid Helianthus sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In Zymoseptoria fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid Xiphophorus swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, genetic drift will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not homozygous for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative overdominance,<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi,<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus,<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in Mus domesticus house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in Heliconius butterflies<ref name=":79" /> and in Xiphophorus swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in Xipophorous fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in Mimulus plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure3_Hybrid_genome_stabilization.jpg|thumb|229x229px|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce chromosomal rearrangements.<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis,<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some Heliconius species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. F.|date=2009|editor-last=Nachman|editor-first=Michael W.|title=The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing|url=https://dx.plos.org/10.1371/journal.pgen.1000550|journal=PLoS Genetics|language=en|volume=5|issue=7|pages=e1000550|doi=10.1371/journal.pgen.1000550|issn=1553-7404|pmc=PMC2696600|pmid=19578407}}</ref><ref name=":147">{{Citation|last=Green|first=R. E.|last2=Krause|first2=J.|last3=Briggs|first3=A. W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> 9v20rhtkfogr6ob0f2w3890gf38mij2 8076 8075 2019-08-12T13:01:15Z Annarunemark 132 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and [[w:Hybridisation_(biology)|hybridization]] between recently diverged species can lead to loss of genetic [[w:adaptation|adaptation]]s or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted [[w:supergene|gene complex]]es.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> ''Heliconius'' butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian ''Madiinae'' tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to [[w:reinforcement speciation|reinforcement]], selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids [[w:backcrossing|backcrosssing]] with parental species. Such introgressive hybridization may enable neutral or selectively beneficial [[w:allele|allele]]s to be transferred across species boundaries even in species pairs that remain distinct despite occasional [[w:gene flow|gene flow]].<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid [[w:fitness biology|fitness]] may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including ''Drosophila'',<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with [[w:reproductive isolation|reproductive isolation]] to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />)) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive [[w:loci|loci]] are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include an insecticide resistance gene that was transferred from ''Anopheles gambiae'' to ''A. coluzzii''<ref name=":20" /> and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta''<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other ''Heliconius'' species.<ref name=":19" /> In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and [[w:phytotoxicity|phytotoxic]] levels of metal have been introgressed from ''A. lyrata''.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolated against other populations of the same species. Examples of this include ''Heliconius'' butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between ''H. t. florencia'' and ''H. t. linaresi'') and intermediate levels (e.g. ''H. c. galanthus''/''H. pachinus'') of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. ''Heliconius heurippa'',<ref name=":9" /><ref name=":10" /><ref name=":11" /> ''Passer italiae'',<ref name=":27" /> and three ''Helianthus'' sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication ([[w:polyploidy|polyploidy]]) or not. Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination.<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an allopolyploid with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, autopolyploids are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences.<ref name=":49" /> [[File:Figure2_Homoploid_and_allopolyploid_hybridization.svg|link=Special:FilePath/Figure2_Homoploid_and_allopolyploid_hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental condictions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic have been shown to isolate the hybrid species Senecio eboracensis from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that selfing, timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in Geospiza Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid Heliconius butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in Rhagoletis pomonella maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In Xiphophorus swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on Helianthus sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow Passer italiae and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and linkage among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through transgressive phenotypes,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome.<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid Helianthus sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In Zymoseptoria fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid Xiphophorus swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, genetic drift will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not homozygous for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative overdominance,<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi,<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus,<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in Mus domesticus house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in Heliconius butterflies<ref name=":79" /> and in Xiphophorus swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in Xipophorous fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in Mimulus plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure3_Hybrid_genome_stabilization.jpg|thumb|229x229px|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce chromosomal rearrangements.<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis,<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some Heliconius species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. F.|date=2009|editor-last=Nachman|editor-first=Michael W.|title=The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing|url=https://dx.plos.org/10.1371/journal.pgen.1000550|journal=PLoS Genetics|language=en|volume=5|issue=7|pages=e1000550|doi=10.1371/journal.pgen.1000550|issn=1553-7404|pmc=PMC2696600|pmid=19578407}}</ref><ref name=":147">{{Citation|last=Green|first=R. E.|last2=Krause|first2=J.|last3=Briggs|first3=A. W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> o9npppvztzq1vtjtkrn0c1nzlhn61pg 8077 8076 2019-08-12T14:31:04Z Annarunemark 132 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and [[w:Hybridisation_(biology)|hybridization]] between recently diverged species can lead to loss of genetic [[w:adaptation|adaptation]]s or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted [[w:supergene|gene complex]]es.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> ''Heliconius'' butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian ''Madiinae'' tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to [[w:reinforcement speciation|reinforcement]], selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids [[w:backcrossing|backcrosssing]] with parental species. Such introgressive hybridization may enable neutral or selectively beneficial [[w:allele|allele]]s to be transferred across species boundaries even in species pairs that remain distinct despite occasional [[w:gene flow|gene flow]].<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid [[w:fitness biology|fitness]] may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including ''Drosophila'',<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with [[w:reproductive isolation|reproductive isolation]] to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />)) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive [[w:loci|loci]] are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include an insecticide resistance gene that was transferred from ''Anopheles gambiae'' to ''A. coluzzii''<ref name=":20" /> and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta''<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other ''Heliconius'' species.<ref name=":19" /> In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and [[w:phytotoxicity|phytotoxic]] levels of metal have been introgressed from ''A. lyrata''.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolated against other populations of the same species. Examples of this include ''Heliconius'' butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between ''H. t. florencia'' and ''H. t. linaresi'') and intermediate levels (e.g. ''H. c. galanthus''/''H. pachinus'') of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. ''Heliconius heurippa'',<ref name=":9" /><ref name=":10" /><ref name=":11" /> ''Passer italiae'',<ref name=":27" /> and three ''Helianthus'' sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication ([[w:polyploidy|polyploidy]]) or not. Homoploid hybrid speciation [[w:hybrid speciation|Homoploid hybrid speciation]] is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by [[w:recombination (genetic)|recombination]].<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an [[w:polyploidy:allopolyploid]] with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, [[w:polyploidy:autopolyploid]]s are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through [[w:chromosome:chromosome]] number differences.<ref name=":49" /> [[File:Figure2_Homoploid_and_allopolyploid_hybridization.svg|link=Special:FilePath/Figure2_Homoploid_and_allopolyploid_hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where [[w:karyotype|karyotype]] differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental conditions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic has been shown to isolate the hybrid species ''Senecio eboracensis'' from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that [[w:selfing|selfing]], timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in ''Geospiza'' Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in ''Rhagoletis pomonella'' maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on ''Helianthus'' sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow ''Passer italiae'' and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and [[w:genetic linkage:linkage]] among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through [[w:transgressive segregation|transgressive phenotype]]s,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, [[w:recombination (genetic)|recombination]] can destabilize the [[w:karyotype|karyotype]] and lead to aberrant [[w:meiosis|meiotic]] behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, [[w:dominance(genetics)|dominance]], and whether the locus was situated on an [[w:autosome|autosome]] or [[w:sex chromosome|sex chromosome]].<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid ''Xiphophorus'' swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, [[w:genetic drift|genetic drift]] will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not homozygous for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative overdominance,<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi,<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus,<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in Mus domesticus house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in Heliconius butterflies<ref name=":79" /> and in Xiphophorus swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in Xipophorous fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in Mimulus plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure3_Hybrid_genome_stabilization.jpg|thumb|229x229px|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce chromosomal rearrangements.<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis,<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some Heliconius species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. 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W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> gc3o2r3wd6annm21dpec7abl9pk7u54 8078 8077 2019-08-12T14:34:25Z Annarunemark 132 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and [[w:Hybridisation_(biology)|hybridization]] between recently diverged species can lead to loss of genetic [[w:adaptation|adaptation]]s or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted [[w:supergene|gene complex]]es.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> ''Heliconius'' butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian ''Madiinae'' tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to [[w:reinforcement speciation|reinforcement]], selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids [[w:backcrossing|backcrosssing]] with parental species. Such introgressive hybridization may enable neutral or selectively beneficial [[w:allele|allele]]s to be transferred across species boundaries even in species pairs that remain distinct despite occasional [[w:gene flow|gene flow]].<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid [[w:fitness biology|fitness]] may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including ''Drosophila'',<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with [[w:reproductive isolation|reproductive isolation]] to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />)) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive [[w:loci|loci]] are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include an insecticide resistance gene that was transferred from ''Anopheles gambiae'' to ''A. coluzzii''<ref name=":20" /> and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta''<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other ''Heliconius'' species.<ref name=":19" /> In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and [[w:phytotoxicity|phytotoxic]] levels of metal have been introgressed from ''A. lyrata''.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolated against other populations of the same species. Examples of this include ''Heliconius'' butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between ''H. t. florencia'' and ''H. t. linaresi'') and intermediate levels (e.g. ''H. c. galanthus''/''H. pachinus'') of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. ''Heliconius heurippa'',<ref name=":9" /><ref name=":10" /><ref name=":11" /> ''Passer italiae'',<ref name=":27" /> and three ''Helianthus'' sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication ([[w:polyploidy|polyploidy]]) or not. Homoploid hybrid speciation [[w:hybrid speciation|Homoploid hybrid speciation]] is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by [[w:recombination (genetic)|recombination]].<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an [[w:allopolyploid|allopolyploid]] with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, [[w:autopolyploid|autopolyploid]]s are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through [[w:chromosome:chromosome]] number differences.<ref name=":49" /> [[File:Figure2_Homoploid_and_allopolyploid_hybridization.svg|link=Special:FilePath/Figure2_Homoploid_and_allopolyploid_hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where [[w:karyotype|karyotype]] differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental conditions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic has been shown to isolate the hybrid species ''Senecio eboracensis'' from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that [[w:selfing|selfing]], timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in ''Geospiza'' Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in ''Rhagoletis pomonella'' maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on ''Helianthus'' sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow ''Passer italiae'' and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and [[w:genetic linkage:linkage]] among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through [[w:transgressive segregation|transgressive phenotype]]s,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, [[w:recombination (genetic)|recombination]] can destabilize the [[w:karyotype|karyotype]] and lead to aberrant [[w:meiosis|meiotic]] behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, [[w:dominance(genetics)|dominance]], and whether the locus was situated on an [[w:autosome|autosome]] or [[w:sex chromosome|sex chromosome]].<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid ''Xiphophorus'' swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, [[w:genetic drift|genetic drift]] will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not homozygous for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative overdominance,<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi,<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus,<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in Mus domesticus house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in Heliconius butterflies<ref name=":79" /> and in Xiphophorus swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in Xipophorous fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in Mimulus plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure3_Hybrid_genome_stabilization.jpg|thumb|229x229px|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce chromosomal rearrangements.<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis,<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some Heliconius species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. F.|date=2009|editor-last=Nachman|editor-first=Michael W.|title=The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing|url=https://dx.plos.org/10.1371/journal.pgen.1000550|journal=PLoS Genetics|language=en|volume=5|issue=7|pages=e1000550|doi=10.1371/journal.pgen.1000550|issn=1553-7404|pmc=PMC2696600|pmid=19578407}}</ref><ref name=":147">{{Citation|last=Green|first=R. E.|last2=Krause|first2=J.|last3=Briggs|first3=A. W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> 7iscw0i4ru3tlxskdj6mmxz9qntbeu3 8079 8078 2019-08-12T14:46:43Z Annarunemark 132 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and [[w:Hybridisation_(biology)|hybridization]] between recently diverged species can lead to loss of genetic [[w:adaptation|adaptation]]s or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted [[w:supergene|gene complex]]es.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> ''Heliconius'' butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian ''Madiinae'' tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to [[w:reinforcement speciation|reinforcement]], selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids [[w:backcrossing|backcrosssing]] with parental species. Such introgressive hybridization may enable neutral or selectively beneficial [[w:allele|allele]]s to be transferred across species boundaries even in species pairs that remain distinct despite occasional [[w:gene flow|gene flow]].<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid [[w:fitness biology|fitness]] may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including ''Drosophila'',<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with [[w:reproductive isolation|reproductive isolation]] to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />)) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive [[w:loci|loci]] are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include an insecticide resistance gene that was transferred from ''Anopheles gambiae'' to ''A. coluzzii''<ref name=":20" /> and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta''<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other ''Heliconius'' species.<ref name=":19" /> In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and [[w:phytotoxicity|phytotoxic]] levels of metal have been introgressed from ''A. lyrata''.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolated against other populations of the same species. Examples of this include ''Heliconius'' butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between ''H. t. florencia'' and ''H. t. linaresi'') and intermediate levels (e.g. ''H. c. galanthus''/''H. pachinus'') of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. ''Heliconius heurippa'',<ref name=":9" /><ref name=":10" /><ref name=":11" /> ''Passer italiae'',<ref name=":27" /> and three ''Helianthus'' sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication ([[w:polyploidy|polyploidy]]) or not. Homoploid hybrid speciation [[w:hybrid speciation|Homoploid hybrid speciation]] is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by [[w:recombination (genetic)|recombination]].<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an [[w:allopolyploid|allopolyploid]] with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, [[w:autopolyploid|autopolyploid]]s are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through [[w:chromosome|chromosome]] number differences.<ref name=":49" /> [[File:Figure2_Homoploid_and_allopolyploid_hybridization.svg|link=Special:FilePath/Figure2_Homoploid_and_allopolyploid_hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where [[w:karyotype|karyotype]] differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental conditions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic has been shown to isolate the hybrid species ''Senecio eboracensis'' from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that [[w:selfing|selfing]], timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in ''Geospiza'' Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in ''Rhagoletis pomonella'' maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on ''Helianthus'' sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow ''Passer italiae'' and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and [[w:genetic linkage:linkage]] among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through [[w:transgressive segregation|transgressive phenotype]]s,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, [[w:recombination (genetic)|recombination]] can destabilize the [[w:karyotype|karyotype]] and lead to aberrant [[w:meiosis|meiotic]] behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, [[w:dominance(genetics)|dominance]], and whether the locus was situated on an [[w:autosome|autosome]] or [[w:sex chromosome|sex chromosome]].<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid ''Xiphophorus'' swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, [[w:genetic drift|genetic drift]] will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not [[w:homozygous|homozygous]] for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative [[w:overdominance|overdominance]],<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in ''Anopheles coluzzi'',<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local [[w:recombination frequency|recombination rate]] is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers ''Mimulus'',<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in ''Mus domesticus'' house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in ''Heliconius'' butterflies<ref name=":79" /> and in ''Xiphophorus'' swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in ''Xipophorous'' fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in ''Mimulus'' plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure3_Hybrid_genome_stabilization.jpg|thumb|229x229px|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase [[w:mutation rate|mutation rate]]s,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce [[w:chromosomal rearrangements|chromosomal rearrangements]].<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased [[w:transposon|transposon]] activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana''.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through [[w:diploidization|diploidization]], which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between [[w:homologous chromosomes|homologous chromosomes]] are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of ''Tragopogon miscellus'' show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in [[w:miRNA|miRNA]]s alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of [[w:siRNA|siRNA]]s is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. Haldane’s rule<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidization and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis,<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some Heliconius species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. F.|date=2009|editor-last=Nachman|editor-first=Michael W.|title=The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing|url=https://dx.plos.org/10.1371/journal.pgen.1000550|journal=PLoS Genetics|language=en|volume=5|issue=7|pages=e1000550|doi=10.1371/journal.pgen.1000550|issn=1553-7404|pmc=PMC2696600|pmid=19578407}}</ref><ref name=":147">{{Citation|last=Green|first=R. E.|last2=Krause|first2=J.|last3=Briggs|first3=A. W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> id18970s1twl4icm6k4jllsjzjw2ytu 8080 8079 2019-08-12T15:00:02Z Annarunemark 132 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and [[w:Hybridisation_(biology)|hybridization]] between recently diverged species can lead to loss of genetic [[w:adaptation|adaptation]]s or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted [[w:supergene|gene complex]]es.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> ''Heliconius'' butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian ''Madiinae'' tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to [[w:reinforcement speciation|reinforcement]], selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids [[w:backcrossing|backcrosssing]] with parental species. Such introgressive hybridization may enable neutral or selectively beneficial [[w:allele|allele]]s to be transferred across species boundaries even in species pairs that remain distinct despite occasional [[w:gene flow|gene flow]].<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid [[w:fitness biology|fitness]] may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including ''Drosophila'',<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with [[w:reproductive isolation|reproductive isolation]] to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />)) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive [[w:loci|loci]] are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include an insecticide resistance gene that was transferred from ''Anopheles gambiae'' to ''A. coluzzii''<ref name=":20" /> and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta''<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other ''Heliconius'' species.<ref name=":19" /> In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and [[w:phytotoxicity|phytotoxic]] levels of metal have been introgressed from ''A. lyrata''.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolated against other populations of the same species. Examples of this include ''Heliconius'' butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between ''H. t. florencia'' and ''H. t. linaresi'') and intermediate levels (e.g. ''H. c. galanthus''/''H. pachinus'') of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. ''Heliconius heurippa'',<ref name=":9" /><ref name=":10" /><ref name=":11" /> ''Passer italiae'',<ref name=":27" /> and three ''Helianthus'' sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication ([[w:polyploidy|polyploidy]]) or not. Homoploid hybrid speciation [[w:hybrid speciation|Homoploid hybrid speciation]] is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by [[w:recombination (genetic)|recombination]].<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an [[w:allopolyploid|allopolyploid]] with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, [[w:autopolyploid|autopolyploid]]s are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through [[w:chromosome|chromosome]] number differences.<ref name=":49" /> [[File:Figure2_Homoploid_and_allopolyploid_hybridization.svg|link=Special:FilePath/Figure2_Homoploid_and_allopolyploid_hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where [[w:karyotype|karyotype]] differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental conditions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic has been shown to isolate the hybrid species ''Senecio eboracensis'' from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that [[w:selfing|selfing]], timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in ''Geospiza'' Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in ''Rhagoletis pomonella'' maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on ''Helianthus'' sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow ''Passer italiae'' and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and [[w:genetic linkage|linkage]] among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through [[w:transgressive segregation|transgressive phenotype]]s,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, [[w:recombination (genetic)|recombination]] can destabilize the [[w:karyotype|karyotype]] and lead to aberrant [[w:meiosis|meiotic]] behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, [[w:dominance(genetics)|dominance]], and whether the locus was situated on an [[w:autosome|autosome]] or [[w:sex chromosome|sex chromosome]].<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid ''Xiphophorus'' swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, [[w:genetic drift|genetic drift]] will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not [[w:homozygous|homozygous]] for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative [[w:overdominance|overdominance]],<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in ''Anopheles coluzzi'',<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local [[w:recombination frequency|recombination rate]] is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers ''Mimulus'',<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in ''Mus domesticus'' house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in ''Heliconius'' butterflies<ref name=":79" /> and in ''Xiphophorus'' swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in ''Xipophorous'' fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in ''Mimulus'' plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure3_Hybrid_genome_stabilization.jpg|thumb|229x229px|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase [[w:mutation rate|mutation rate]]s,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce [[w:chromosomal rearrangements|chromosomal rearrangements]].<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased [[w:transposon|transposon]] activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana''.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through [[w:diploidization|diploidization]], which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between [[w:homologous chromosomes|homologous chromosomes]] are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of ''Tragopogon miscellus'' show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in [[w:miRNA|miRNA]]s alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of [[w:siRNA|siRNA]]s is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. [[w:Haldane's rule|Haldane's rule]]<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of [[w:heterogametic sex|heterogametic]] hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to [[w:hemozygosity|hemizygous]] expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of [[w:selfing|selfing]] in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent [[w:parasexual cycle|parasexual]]mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. [[w:polyploidisation|Polyploidisation]] and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare [[w:karyotype|cytotype]]s are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, ''Cobitis'',<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an ''Anopheles gambiae'' resistance allele into ''A. coluzzi'' malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In ''Heliconius'' butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into [[w:secondary contact|secondary contact]]. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some ''Heliconius'' species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for ''Anopheles gambiae'' mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”[[w:super gene|super gene]]” that encodes mimicry polymorphism in the butterfly ''Heliconius numata''.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a ''Mus musculus'' and ''M. domesticus'' hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the ''Nicotiana'' <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. F.|date=2009|editor-last=Nachman|editor-first=Michael W.|title=The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing|url=https://dx.plos.org/10.1371/journal.pgen.1000550|journal=PLoS Genetics|language=en|volume=5|issue=7|pages=e1000550|doi=10.1371/journal.pgen.1000550|issn=1553-7404|pmc=PMC2696600|pmid=19578407}}</ref><ref name=":147">{{Citation|last=Green|first=R. E.|last2=Krause|first2=J.|last3=Briggs|first3=A. W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> 8su12hkjc1nyrudja0r6gujcr830x5k 8081 8080 2019-08-13T06:06:56Z Annarunemark 132 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and [[w:Hybridisation_(biology)|hybridization]] between recently diverged species can lead to loss of genetic [[w:adaptation|adaptation]]s or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted [[w:supergene|gene complex]]es.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> ''Heliconius'' butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian ''Madiinae'' tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to [[w:reinforcement speciation|reinforcement]], selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids [[w:backcrossing|backcrosssing]] with parental species. Such introgressive hybridization may enable neutral or selectively beneficial [[w:allele|allele]]s to be transferred across species boundaries even in species pairs that remain distinct despite occasional [[w:gene flow|gene flow]].<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid [[w:fitness biology|fitness]] may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including ''Drosophila'',<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with [[w:reproductive isolation|reproductive isolation]] to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive [[w:loci|loci]] are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include an insecticide resistance gene that was transferred from ''Anopheles gambiae'' to ''A. coluzzii''<ref name=":20" /> and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta''<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other ''Heliconius'' species.<ref name=":19" /> In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and [[w:phytotoxicity|phytotoxic]] levels of metal have been introgressed from ''A. lyrata''.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolated against other populations of the same species. Examples of this include ''Heliconius'' butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between ''H. t. florencia'' and ''H. t. linaresi'') and intermediate levels (e.g. ''H. c. galanthus''/''H. pachinus'') of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. ''Heliconius heurippa'',<ref name=":9" /><ref name=":10" /><ref name=":11" /> ''Passer italiae'',<ref name=":27" /> and three ''Helianthus'' sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication ([[w:polyploidy|polyploidy]]) or not. Homoploid hybrid speciation [[w:hybrid speciation|Homoploid hybrid speciation]] is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by [[w:recombination (genetic)|recombination]].<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an [[w:allopolyploid|allopolyploid]] with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, [[w:autopolyploid|autopolyploid]]s are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through [[w:chromosome|chromosome]] number differences.<ref name=":49" /> [[File:Figure2_Homoploid_and_allopolyploid_hybridization.svg|link=Special:FilePath/Figure2_Homoploid_and_allopolyploid_hybridization.svg|thumb|Figure 2. Schematic representations of homoploid hybrid speciation and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where [[w:karyotype|karyotype]] differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental conditions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic has been shown to isolate the hybrid species ''Senecio eboracensis'' from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that [[w:selfing|selfing]], timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in ''Geospiza'' Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in ''Rhagoletis pomonella'' maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on ''Helianthus'' sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow ''Passer italiae'' and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and [[w:genetic linkage|linkage]] among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through [[w:transgressive segregation|transgressive phenotype]]s,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, [[w:recombination (genetic)|recombination]] can destabilize the [[w:karyotype|karyotype]] and lead to aberrant [[w:meiosis|meiotic]] behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, [[w:dominance(genetics)|dominance]], and whether the locus was situated on an [[w:autosome|autosome]] or [[w:sex chromosome|sex chromosome]].<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid ''Xiphophorus'' swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, [[w:genetic drift|genetic drift]] will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not [[w:homozygous|homozygous]] for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative [[w:overdominance|overdominance]],<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in ''Anopheles coluzzi'',<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local [[w:recombination frequency|recombination rate]] is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers ''Mimulus'',<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in ''Mus domesticus'' house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in ''Heliconius'' butterflies<ref name=":79" /> and in ''Xiphophorus'' swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in ''Xipophorous'' fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in ''Mimulus'' plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure3_Hybrid_genome_stabilization.jpg|thumb|229x229px|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase [[w:mutation rate|mutation rate]]s,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce [[w:chromosomal rearrangements|chromosomal rearrangements]].<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased [[w:transposon|transposon]] activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana''.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through [[w:diploidization|diploidization]], which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between [[w:homologous chromosomes|homologous chromosomes]] are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of ''Tragopogon miscellus'' show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in [[w:miRNA|miRNA]]s alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of [[w:siRNA|siRNA]]s is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. [[w:Haldane's rule|Haldane's rule]]<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of [[w:heterogametic sex|heterogametic]] hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to [[w:hemozygosity|hemizygous]] expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of [[w:selfing|selfing]] in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent [[w:parasexual cycle|parasexual]] mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. [[w:polyploidisation|Polyploidisation]] and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare [[w:karyotype|cytotype]]s are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, ''Cobitis'',<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an ''Anopheles gambiae'' resistance allele into ''A. coluzzi'' malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In ''Heliconius'' butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into [[w:secondary contact|secondary contact]]. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some ''Heliconius'' species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for ''Anopheles gambiae'' mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”[[w:super gene|super gene]]” that encodes mimicry polymorphism in the butterfly ''Heliconius numata''.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a ''Mus musculus'' and ''M. domesticus'' hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the ''Nicotiana'' <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. F.|date=2009|editor-last=Nachman|editor-first=Michael W.|title=The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing|url=https://dx.plos.org/10.1371/journal.pgen.1000550|journal=PLoS Genetics|language=en|volume=5|issue=7|pages=e1000550|doi=10.1371/journal.pgen.1000550|issn=1553-7404|pmc=PMC2696600|pmid=19578407}}</ref><ref name=":147">{{Citation|last=Green|first=R. E.|last2=Krause|first2=J.|last3=Briggs|first3=A. W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> 71lx2t35l1vfg8k9tsbwpp6qvhtyke4 8082 8081 2019-08-13T07:03:43Z Annarunemark 132 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and [[w:Hybridisation_(biology)|hybridization]] between recently diverged species can lead to loss of genetic [[w:adaptation|adaptation]]s or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted [[w:supergene|gene complex]]es.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> ''Heliconius'' butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian ''Madiinae'' tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to [[w:reinforcement speciation|reinforcement]], selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids [[w:backcrossing|backcrosssing]] with parental species. Such introgressive hybridization may enable neutral or selectively beneficial [[w:allele|allele]]s to be transferred across species boundaries even in species pairs that remain distinct despite occasional [[w:gene flow|gene flow]].<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid [[w:fitness biology|fitness]] may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including ''Drosophila'',<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with [[w:reproductive isolation|reproductive isolation]] to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive [[w:loci|loci]] are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include an insecticide resistance gene that was transferred from ''Anopheles gambiae'' to ''A. coluzzii''<ref name=":20" /> and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta''<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other ''Heliconius'' species.<ref name=":19" /> In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and [[w:phytotoxicity|phytotoxic]] levels of metal have been introgressed from ''A. lyrata''.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolated against other populations of the same species. Examples of this include ''Heliconius'' butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between ''H. t. florencia'' and ''H. t. linaresi'') and intermediate levels (e.g. ''H. c. galanthus''/''H. pachinus'') of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. ''Heliconius heurippa'',<ref name=":9" /><ref name=":10" /><ref name=":11" /> ''Passer italiae'',<ref name=":27" /> and three ''Helianthus'' sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication ([[w:polyploidy|polyploidy]]) or not. Homoploid hybrid speciation [[w:hybrid speciation|Homoploid hybrid speciation]] is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by [[w:recombination (genetic)|recombination]].<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an [[w:allopolyploid|allopolyploid]] with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, [[w:autopolyploid|autopolyploid]]s are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through [[w:chromosome|chromosome]] number differences.<ref name=":49" /> [[File:Figure 2. Schematic representation of homoploid and allopolyploid hybrid speciation. Updated.svg|thumb|Figure 2. Schematic representation of homoploid and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where [[w:karyotype|karyotype]] differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental conditions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic has been shown to isolate the hybrid species ''Senecio eboracensis'' from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that [[w:selfing|selfing]], timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in ''Geospiza'' Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in ''Rhagoletis pomonella'' maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on ''Helianthus'' sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow ''Passer italiae'' and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and [[w:genetic linkage|linkage]] among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through [[w:transgressive segregation|transgressive phenotype]]s,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, [[w:recombination (genetic)|recombination]] can destabilize the [[w:karyotype|karyotype]] and lead to aberrant [[w:meiosis|meiotic]] behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, [[w:dominance(genetics)|dominance]], and whether the locus was situated on an [[w:autosome|autosome]] or [[w:sex chromosome|sex chromosome]].<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid ''Xiphophorus'' swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, [[w:genetic drift|genetic drift]] will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not [[w:homozygous|homozygous]] for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative [[w:overdominance|overdominance]],<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in ''Anopheles coluzzi'',<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local [[w:recombination frequency|recombination rate]] is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers ''Mimulus'',<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in ''Mus domesticus'' house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in ''Heliconius'' butterflies<ref name=":79" /> and in ''Xiphophorus'' swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in ''Xipophorous'' fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in ''Mimulus'' plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure3_Hybrid_genome_stabilization.jpg|thumb|229x229px|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase [[w:mutation rate|mutation rate]]s,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce [[w:chromosomal rearrangements|chromosomal rearrangements]].<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased [[w:transposon|transposon]] activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana''.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through [[w:diploidization|diploidization]], which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between [[w:homologous chromosomes|homologous chromosomes]] are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of ''Tragopogon miscellus'' show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in [[w:miRNA|miRNA]]s alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of [[w:siRNA|siRNA]]s is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. [[w:Haldane's rule|Haldane's rule]]<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of [[w:heterogametic sex|heterogametic]] hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to [[w:hemozygosity|hemizygous]] expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of [[w:selfing|selfing]] in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent [[w:parasexual cycle|parasexual]] mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. [[w:polyploidisation|Polyploidisation]] and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare [[w:karyotype|cytotype]]s are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, ''Cobitis'',<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an ''Anopheles gambiae'' resistance allele into ''A. coluzzi'' malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In ''Heliconius'' butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into [[w:secondary contact|secondary contact]]. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some ''Heliconius'' species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for ''Anopheles gambiae'' mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”[[w:super gene|super gene]]” that encodes mimicry polymorphism in the butterfly ''Heliconius numata''.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a ''Mus musculus'' and ''M. domesticus'' hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the ''Nicotiana'' <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. F.|date=2009|editor-last=Nachman|editor-first=Michael W.|title=The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing|url=https://dx.plos.org/10.1371/journal.pgen.1000550|journal=PLoS Genetics|language=en|volume=5|issue=7|pages=e1000550|doi=10.1371/journal.pgen.1000550|issn=1553-7404|pmc=PMC2696600|pmid=19578407}}</ref><ref name=":147">{{Citation|last=Green|first=R. E.|last2=Krause|first2=J.|last3=Briggs|first3=A. W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> a98yaxpzcm3cwtvt9fn5svw2d6yi6rp 8083 8082 2019-08-13T07:27:21Z Annarunemark 132 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and [[w:Hybridisation_(biology)|hybridization]] between recently diverged species can lead to loss of genetic [[w:adaptation|adaptation]]s or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted [[w:supergene|gene complex]]es.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> ''Heliconius'' butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian ''Madiinae'' tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to [[w:reinforcement speciation|reinforcement]], selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids [[w:backcrossing|backcrosssing]] with parental species. Such introgressive hybridization may enable neutral or selectively beneficial [[w:allele|allele]]s to be transferred across species boundaries even in species pairs that remain distinct despite occasional [[w:gene flow|gene flow]].<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid [[w:fitness biology|fitness]] may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including ''Drosophila'',<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with [[w:reproductive isolation|reproductive isolation]] to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive [[w:loci|loci]] are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include an insecticide resistance gene that was transferred from ''Anopheles gambiae'' to ''A. coluzzii''<ref name=":20" /> and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta''<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other ''Heliconius'' species.<ref name=":19" /> In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and [[w:phytotoxicity|phytotoxic]] levels of metal have been introgressed from ''A. lyrata''.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolated against other populations of the same species. Examples of this include ''Heliconius'' butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between ''H. t. florencia'' and ''H. t. linaresi'') and intermediate levels (e.g. ''H. c. galanthus''/''H. pachinus'') of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. ''Heliconius heurippa'',<ref name=":9" /><ref name=":10" /><ref name=":11" /> ''Passer italiae'',<ref name=":27" /> and three ''Helianthus'' sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication ([[w:polyploidy|polyploidy]]) or not. Homoploid hybrid speciation [[w:hybrid speciation|Homoploid hybrid speciation]] is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by [[w:recombination (genetic)|recombination]].<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an [[w:allopolyploid|allopolyploid]] with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, [[w:autopolyploid|autopolyploid]]s are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through [[w:chromosome|chromosome]] number differences.<ref name=":49" /> [[File:Figure 2. Schematic representation of homoploid and allopolyploid hybrid speciation. Updated.svg|thumb|Figure 2. Schematic representation of homoploid and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where [[w:karyotype|karyotype]] differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental conditions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic has been shown to isolate the hybrid species ''Senecio eboracensis'' from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that [[w:selfing|selfing]], timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in ''Geospiza'' Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in ''Rhagoletis pomonella'' maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on ''Helianthus'' sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow ''Passer italiae'' and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and [[w:genetic linkage|linkage]] among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through [[w:transgressive segregation|transgressive phenotype]]s,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, [[w:recombination (genetic)|recombination]] can destabilize the [[w:karyotype|karyotype]] and lead to aberrant [[w:meiosis|meiotic]] behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, [[w:dominance(genetics)|dominance]], and whether the locus was situated on an [[w:autosome|autosome]] or [[w:sex chromosome|sex chromosome]].<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid ''Xiphophorus'' swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, [[w:genetic drift|genetic drift]] will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not [[w:homozygous|homozygous]] for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative [[w:overdominance|overdominance]],<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in ''Anopheles coluzzi'',<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local [[w:recombination frequency|recombination rate]] is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers ''Mimulus'',<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in ''Mus domesticus'' house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in ''Heliconius'' butterflies<ref name=":79" /> and in ''Xiphophorus'' swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in ''Xipophorous'' fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in ''Mimulus'' plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure3_Hybrid_genome_stabilization.jpg|thumb|229x229px|Figure 3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase [[w:mutation rate|mutation rate]]s,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce [[w:chromosomal rearrangements|chromosomal rearrangements]].<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased [[w:transposon|transposon]] activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana''.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through [[w:diploidization|diploidization]], which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between [[w:homologous chromosomes|homologous chromosomes]] are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of ''Tragopogon miscellus'' show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in [[w:miRNA|miRNA]]s alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of [[w:siRNA|siRNA]]s is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. [[w:Haldane's rule|Haldane's rule]]<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of [[w:heterogametic sex|heterogametic]] hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to [[w:hemozygosity|hemizygous]] expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of [[w:selfing|selfing]] in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent [[w:parasexual cycle|parasexual]] mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. [[w:polyploidisation|Polyploidisation]] and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare [[w:karyotype|cytotype]]s are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, ''Cobitis'',<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an ''Anopheles gambiae'' resistance allele into ''A. coluzzi'' malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In ''Heliconius'' butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into [[w:secondary contact|secondary contact]]. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some ''Heliconius'' species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for ''Anopheles gambiae'' mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”[[w:super gene|super gene]]” that encodes mimicry polymorphism in the butterfly ''Heliconius numata''.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a ''Mus musculus'' and ''M. domesticus'' hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the ''Nicotiana'' <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. F.|date=2009|editor-last=Nachman|editor-first=Michael W.|title=The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing|url=https://dx.plos.org/10.1371/journal.pgen.1000550|journal=PLoS Genetics|language=en|volume=5|issue=7|pages=e1000550|doi=10.1371/journal.pgen.1000550|issn=1553-7404|pmc=PMC2696600|pmid=19578407}}</ref><ref name=":147">{{Citation|last=Green|first=R. E.|last2=Krause|first2=J.|last3=Briggs|first3=A. W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> hpxfprvqsm7if747vyjzfhej9at24mq 8085 8083 2019-08-13T10:22:59Z Annarunemark 132 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and [[w:Hybridisation_(biology)|hybridization]] between recently diverged species can lead to loss of genetic [[w:adaptation|adaptation]]s or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted [[w:supergene|gene complex]]es.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> ''Heliconius'' butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian ''Madiinae'' tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to [[w:reinforcement speciation|reinforcement]], selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids [[w:backcrossing|backcrosssing]] with parental species. Such introgressive hybridization may enable neutral or selectively beneficial [[w:allele|allele]]s to be transferred across species boundaries even in species pairs that remain distinct despite occasional [[w:gene flow|gene flow]].<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid [[w:fitness biology|fitness]] may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including ''Drosophila'',<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with [[w:reproductive isolation|reproductive isolation]] to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive [[w:loci|loci]] are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include an insecticide resistance gene that was transferred from ''Anopheles gambiae'' to ''A. coluzzii''<ref name=":20" /> and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta''<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other ''Heliconius'' species.<ref name=":19" /> In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and [[w:phytotoxicity|phytotoxic]] levels of metal have been introgressed from ''A. lyrata''.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolated against other populations of the same species. Examples of this include ''Heliconius'' butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between ''H. t. florencia'' and ''H. t. linaresi'') and intermediate levels (e.g. ''H. c. galanthus''/''H. pachinus'') of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. ''Heliconius heurippa'',<ref name=":9" /><ref name=":10" /><ref name=":11" /> ''Passer italiae'',<ref name=":27" /> and three ''Helianthus'' sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication ([[w:polyploidy|polyploidy]]) or not. Homoploid hybrid speciation [[w:hybrid speciation|Homoploid hybrid speciation]] is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by [[w:recombination (genetic)|recombination]].<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an [[w:allopolyploid|allopolyploid]] with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, [[w:autopolyploid|autopolyploid]]s are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through [[w:chromosome|chromosome]] number differences.<ref name=":49" /> [[File:Figure 2. Schematic representation of homoploid and allopolyploid hybrid speciation. Updated.svg|thumb|Figure 2. Schematic representation of homoploid and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where [[w:karyotype|karyotype]] differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental conditions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic has been shown to isolate the hybrid species ''Senecio eboracensis'' from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that [[w:selfing|selfing]], timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in ''Geospiza'' Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in ''Rhagoletis pomonella'' maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on ''Helianthus'' sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow ''Passer italiae'' and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and [[w:genetic linkage|linkage]] among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through [[w:transgressive segregation|transgressive phenotype]]s,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, [[w:recombination (genetic)|recombination]] can destabilize the [[w:karyotype|karyotype]] and lead to aberrant [[w:meiosis|meiotic]] behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, [[w:dominance(genetics)|dominance]], and whether the locus was situated on an [[w:autosome|autosome]] or [[w:sex chromosome|sex chromosome]].<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid ''Xiphophorus'' swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, [[w:genetic drift|genetic drift]] will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not [[w:homozygous|homozygous]] for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative [[w:overdominance|overdominance]],<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in ''Anopheles coluzzi'',<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local [[w:recombination frequency|recombination rate]] is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers ''Mimulus'',<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in ''Mus domesticus'' house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in ''Heliconius'' butterflies<ref name=":79" /> and in ''Xiphophorus'' swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in ''Xipophorous'' fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in ''Mimulus'' plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure 3. The process of genome stabilization during hybrid speciation and introgression.svg|thumb|The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase [[w:mutation rate|mutation rate]]s,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce [[w:chromosomal rearrangements|chromosomal rearrangements]].<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased [[w:transposon|transposon]] activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana''.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through [[w:diploidization|diploidization]], which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between [[w:homologous chromosomes|homologous chromosomes]] are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of ''Tragopogon miscellus'' show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in [[w:miRNA|miRNA]]s alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of [[w:siRNA|siRNA]]s is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. [[w:Haldane's rule|Haldane's rule]]<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of [[w:heterogametic sex|heterogametic]] hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to [[w:hemozygosity|hemizygous]] expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of [[w:selfing|selfing]] in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent [[w:parasexual cycle|parasexual]] mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. [[w:polyploidisation|Polyploidisation]] and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare [[w:karyotype|cytotype]]s are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, ''Cobitis'',<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an ''Anopheles gambiae'' resistance allele into ''A. coluzzi'' malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In ''Heliconius'' butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into [[w:secondary contact|secondary contact]]. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some ''Heliconius'' species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for ''Anopheles gambiae'' mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”[[w:super gene|super gene]]” that encodes mimicry polymorphism in the butterfly ''Heliconius numata''.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a ''Mus musculus'' and ''M. domesticus'' hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the ''Nicotiana'' <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. F.|date=2009|editor-last=Nachman|editor-first=Michael W.|title=The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing|url=https://dx.plos.org/10.1371/journal.pgen.1000550|journal=PLoS Genetics|language=en|volume=5|issue=7|pages=e1000550|doi=10.1371/journal.pgen.1000550|issn=1553-7404|pmc=PMC2696600|pmid=19578407}}</ref><ref name=":147">{{Citation|last=Green|first=R. E.|last2=Krause|first2=J.|last3=Briggs|first3=A. W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> r3qny4lpu5ngqsggd2yrc6sxnztxtum 8086 8085 2019-08-13T10:23:55Z Annarunemark 132 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and [[w:Hybridisation_(biology)|hybridization]] between recently diverged species can lead to loss of genetic [[w:adaptation|adaptation]]s or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted [[w:supergene|gene complex]]es.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> ''Heliconius'' butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian ''Madiinae'' tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to [[w:reinforcement speciation|reinforcement]], selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids [[w:backcrossing|backcrosssing]] with parental species. Such introgressive hybridization may enable neutral or selectively beneficial [[w:allele|allele]]s to be transferred across species boundaries even in species pairs that remain distinct despite occasional [[w:gene flow|gene flow]].<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid [[w:fitness biology|fitness]] may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including ''Drosophila'',<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with [[w:reproductive isolation|reproductive isolation]] to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive [[w:loci|loci]] are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include an insecticide resistance gene that was transferred from ''Anopheles gambiae'' to ''A. coluzzii''<ref name=":20" /> and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta''<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other ''Heliconius'' species.<ref name=":19" /> In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and [[w:phytotoxicity|phytotoxic]] levels of metal have been introgressed from ''A. lyrata''.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolated against other populations of the same species. Examples of this include ''Heliconius'' butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between ''H. t. florencia'' and ''H. t. linaresi'') and intermediate levels (e.g. ''H. c. galanthus''/''H. pachinus'') of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. ''Heliconius heurippa'',<ref name=":9" /><ref name=":10" /><ref name=":11" /> ''Passer italiae'',<ref name=":27" /> and three ''Helianthus'' sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication ([[w:polyploidy|polyploidy]]) or not. Homoploid hybrid speciation [[w:hybrid speciation|Homoploid hybrid speciation]] is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by [[w:recombination (genetic)|recombination]].<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an [[w:allopolyploid|allopolyploid]] with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, [[w:autopolyploid|autopolyploid]]s are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through [[w:chromosome|chromosome]] number differences.<ref name=":49" /> [[File:Figure 2. Schematic representation of homoploid and allopolyploid hybrid speciation. Updated.svg|thumb|Figure 2. Schematic representation of homoploid and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where [[w:karyotype|karyotype]] differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental conditions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic has been shown to isolate the hybrid species ''Senecio eboracensis'' from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that [[w:selfing|selfing]], timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in ''Geospiza'' Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in ''Rhagoletis pomonella'' maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on ''Helianthus'' sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow ''Passer italiae'' and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and [[w:genetic linkage|linkage]] among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through [[w:transgressive segregation|transgressive phenotype]]s,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, [[w:recombination (genetic)|recombination]] can destabilize the [[w:karyotype|karyotype]] and lead to aberrant [[w:meiosis|meiotic]] behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, [[w:dominance(genetics)|dominance]], and whether the locus was situated on an [[w:autosome|autosome]] or [[w:sex chromosome|sex chromosome]].<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid ''Xiphophorus'' swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, [[w:genetic drift|genetic drift]] will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not [[w:homozygous|homozygous]] for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative [[w:overdominance|overdominance]],<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in ''Anopheles coluzzi'',<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local [[w:recombination frequency|recombination rate]] is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers ''Mimulus'',<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in ''Mus domesticus'' house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in ''Heliconius'' butterflies<ref name=":79" /> and in ''Xiphophorus'' swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in ''Xipophorous'' fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in ''Mimulus'' plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure 3. Figure3. The process of genome stabilization during hybrid speciation and introgression.svg|thumb|The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase [[w:mutation rate|mutation rate]]s,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce [[w:chromosomal rearrangements|chromosomal rearrangements]].<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased [[w:transposon|transposon]] activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana''.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through [[w:diploidization|diploidization]], which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between [[w:homologous chromosomes|homologous chromosomes]] are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of ''Tragopogon miscellus'' show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in [[w:miRNA|miRNA]]s alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of [[w:siRNA|siRNA]]s is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. [[w:Haldane's rule|Haldane's rule]]<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of [[w:heterogametic sex|heterogametic]] hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to [[w:hemozygosity|hemizygous]] expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of [[w:selfing|selfing]] in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent [[w:parasexual cycle|parasexual]] mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. [[w:polyploidisation|Polyploidisation]] and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare [[w:karyotype|cytotype]]s are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, ''Cobitis'',<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an ''Anopheles gambiae'' resistance allele into ''A. coluzzi'' malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In ''Heliconius'' butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into [[w:secondary contact|secondary contact]]. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some ''Heliconius'' species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for ''Anopheles gambiae'' mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”[[w:super gene|super gene]]” that encodes mimicry polymorphism in the butterfly ''Heliconius numata''.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a ''Mus musculus'' and ''M. domesticus'' hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the ''Nicotiana'' <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. F.|date=2009|editor-last=Nachman|editor-first=Michael W.|title=The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing|url=https://dx.plos.org/10.1371/journal.pgen.1000550|journal=PLoS Genetics|language=en|volume=5|issue=7|pages=e1000550|doi=10.1371/journal.pgen.1000550|issn=1553-7404|pmc=PMC2696600|pmid=19578407}}</ref><ref name=":147">{{Citation|last=Green|first=R. E.|last2=Krause|first2=J.|last3=Briggs|first3=A. W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> k9zc8k3prpeeja6bytt2k9vtcqwd3al 8087 8086 2019-08-13T10:24:50Z Annarunemark 132 wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and [[w:Hybridisation_(biology)|hybridization]] between recently diverged species can lead to loss of genetic [[w:adaptation|adaptation]]s or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted [[w:supergene|gene complex]]es.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''Geospiza'' Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African cichlid fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> ''Heliconius'' butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian ''Madiinae'' tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to [[w:reinforcement speciation|reinforcement]], selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids [[w:backcrossing|backcrosssing]] with parental species. Such introgressive hybridization may enable neutral or selectively beneficial [[w:allele|allele]]s to be transferred across species boundaries even in species pairs that remain distinct despite occasional [[w:gene flow|gene flow]].<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid [[w:fitness biology|fitness]] may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including ''Drosophila'',<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with [[w:reproductive isolation|reproductive isolation]] to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive [[w:loci|loci]] are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include an insecticide resistance gene that was transferred from ''Anopheles gambiae'' to ''A. coluzzii''<ref name=":20" /> and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''H. melpomene'' to ''H. timareta''<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other ''Heliconius'' species.<ref name=":19" /> In the plant ''Arabidopsis arenosa'' some of the alleles conferring adaptation to drought and [[w:phytotoxicity|phytotoxic]] levels of metal have been introgressed from ''A. lyrata''.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolated against other populations of the same species. Examples of this include ''Heliconius'' butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between ''H. t. florencia'' and ''H. t. linaresi'') and intermediate levels (e.g. ''H. c. galanthus''/''H. pachinus'') of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. ''Heliconius heurippa'',<ref name=":9" /><ref name=":10" /><ref name=":11" /> ''Passer italiae'',<ref name=":27" /> and three ''Helianthus'' sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication ([[w:polyploidy|polyploidy]]) or not. Homoploid hybrid speciation [[w:hybrid speciation|Homoploid hybrid speciation]] is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by [[w:recombination (genetic)|recombination]].<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an [[w:allopolyploid|allopolyploid]] with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, [[w:autopolyploid|autopolyploid]]s are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through [[w:chromosome|chromosome]] number differences.<ref name=":49" /> [[File:Figure 2. Schematic representation of homoploid and allopolyploid hybrid speciation. Updated.svg|thumb|Figure 2. Schematic representation of homoploid and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where [[w:karyotype|karyotype]] differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental conditions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic has been shown to isolate the hybrid species ''Senecio eboracensis'' from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that [[w:selfing|selfing]], timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in ''Geospiza'' Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in ''Rhagoletis pomonella'' maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In ''Xiphophorus'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on ''Helianthus'' sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow ''Passer italiae'' and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and [[w:genetic linkage|linkage]] among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through [[w:transgressive segregation|transgressive phenotype]]s,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, [[w:recombination (genetic)|recombination]] can destabilize the [[w:karyotype|karyotype]] and lead to aberrant [[w:meiosis|meiotic]] behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, [[w:dominance(genetics)|dominance]], and whether the locus was situated on an [[w:autosome|autosome]] or [[w:sex chromosome|sex chromosome]].<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid ''Xiphophorus'' swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, [[w:genetic drift|genetic drift]] will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not [[w:homozygous|homozygous]] for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative [[w:overdominance|overdominance]],<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in ''Anopheles coluzzi'',<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local [[w:recombination frequency|recombination rate]] is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers ''Mimulus'',<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in ''Mus domesticus'' house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in ''Heliconius'' butterflies<ref name=":79" /> and in ''Xiphophorus'' swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in ''Xipophorous'' fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in ''Mimulus'' plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure 3. The process of genome stabilization during hybrid speciation and introgression.svg|thumb|Figure3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase [[w:mutation rate|mutation rate]]s,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce [[w:chromosomal rearrangements|chromosomal rearrangements]].<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased [[w:transposon|transposon]] activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana''.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through [[w:diploidization|diploidization]], which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between [[w:homologous chromosomes|homologous chromosomes]] are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of ''Tragopogon miscellus'' show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in [[w:miRNA|miRNA]]s alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of [[w:siRNA|siRNA]]s is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. [[w:Haldane's rule|Haldane's rule]]<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of [[w:heterogametic sex|heterogametic]] hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to [[w:hemozygosity|hemizygous]] expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of [[w:selfing|selfing]] in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent [[w:parasexual cycle|parasexual]] mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. [[w:polyploidisation|Polyploidisation]] and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare [[w:karyotype|cytotype]]s are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, ''Cobitis'',<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an ''Anopheles gambiae'' resistance allele into ''A. coluzzi'' malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In ''Heliconius'' butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into [[w:secondary contact|secondary contact]]. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some ''Heliconius'' species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for ''Anopheles gambiae'' mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”[[w:super gene|super gene]]” that encodes mimicry polymorphism in the butterfly ''Heliconius numata''.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a ''Mus musculus'' and ''M. domesticus'' hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref>. === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f. <ref name=":48" />? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. <ref name=":98" /><ref name=":132" />? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the ''Nicotiana'' <ref name=":99" />? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. F.|date=2009|editor-last=Nachman|editor-first=Michael W.|title=The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing|url=https://dx.plos.org/10.1371/journal.pgen.1000550|journal=PLoS Genetics|language=en|volume=5|issue=7|pages=e1000550|doi=10.1371/journal.pgen.1000550|issn=1553-7404|pmc=PMC2696600|pmid=19578407}}</ref><ref name=":147">{{Citation|last=Green|first=R. E.|last2=Krause|first2=J.|last3=Briggs|first3=A. W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> lnwfrgco485p4zd0y8zijy0f8v1t7lv 8111 8087 2019-09-02T10:36:26Z T Shafee 80 wikilinks of species names wikitext text/x-wiki {{author |first1 = Anna |last1 = Runemark |department1 = Department of Biology |institution1 = [[WP:Lund University|Lund University]] |address1 = 11800 Lund, Sweden |username1 = User:annarunemark |orcid1 = https://orcid.org/0000-0002-8976-5530 |first2 = Mario |last2 = Vallejo-Marin |department2 = Biological and Environmental Sciences |institution2 = [[WP:University of Stirling|University of Stirling]] |address2 = Stirling FK9 4LA, Scotland, UK |username2 = User:Mvallejomarin |orcid2 = https://orcid.org/0000-0002-5663-8025 |first3 = Joana I |last3 = Meier |department3 = Department of Zoology |institution3 = [[WP:University of Cambridge|University of Cambridge]] |address3 = Trinity Lane, Cambridge CB2 1TN, UK |username3 = User:Joanam |orcid3 = https://orcid.org/0000-0001-7726-2875 }} ==Abstract== Interspecific hybridization is the process where closely related [[w:species|species]] mate and produce offspring with [[w:Genetic admixture|admixed genomes]]. The genomic revolution has shown that [[w:Hybridisation_(biology)|hybridization]] is common, and that it may represent an important source of novel [[w:Genetic variation|variation]]. Although most interspecific hybrids are [[w:Hybrid sterility|sterile]] or less fit than their parents, some may survive and reproduce, enabling the [[w:horizontal gene transfer|transfer]] of adaptive variants across the species boundary, and even result in the formation of novel [[w:speciation|evolutionary lineages]]. There are two main variants of hybrid species genomes: [[w:allopolyploid|allopolyploid]], which have one full [[w:Ploidy|chromosome set]] from each parent species, and homoploid, which are a [[w:Mosaic (genetics)|mosaic]] of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of [[w:reproductive isolation|reproductive isolation]] against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel [[w:ecological niche|ecological niche]]s, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in [[w:Fixation (population genetics)|fixation]] of compatible ancestry block combinations within the hybrid species. The potential for rapid [[w:adapation|adapation]] or [[w:speciation|speciation]] makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how [[w:Introgression|introgressed alleles]] or hybrid species can establish and how the resulting hybrid genomes evolve. == Background == Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and [[w:Hybridisation_(biology)|hybridization]] between recently diverged species can lead to loss of genetic [[w:adaptation|adaptation]]s or species fusion.<ref name=":0">{{Citation|last=Abbott|first=R.|last2=Albach|first2=D.|last3=Ansell|first3=S.|last4=Arntzen|first4=J. W.|last5=Baird|first5=S. J. E.|last6=Bierne|first6=N.|last7=Boughman|first7=J.|last8=Brelsford|first8=A.|last9=Buerkle|first9=C. A.|date=2013|title=Hybridization and speciation|url=http://doi.wiley.com/10.1111/j.1420-9101.2012.02599.x|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=229–246|doi=10.1111/j.1420-9101.2012.02599.x}}</ref> Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour<ref name=":1">{{Citation|book|url=http://www.biodiversitylibrary.org/bibliography/27468|title=The genetical theory of natural selection.|last=Fisher|first=Ronald Aylmer|date=1930|publisher=Clarendon Press|location=Oxford|doi=10.5962/bhl.title.27468}}</ref> which can result in breaking up co-adapted [[w:supergene|gene complex]]es.<ref name=":2">{{Citation|book|url=http://www.degruyter.com/view/books/harvard.9780674865327/harvard.9780674865327/harvard.9780674865327.xml|title=Animal Species and Evolution:|last=Mayr|first=Ernst|date=1963|publisher=Harvard University Press|isbn=9780674865327|location=Cambridge, MA and London, England|doi=10.4159/harvard.9780674865327}}</ref> In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity.<ref name=":3">{{Citation|last=Stebbins|first=G. Ledyard|date=1959|title=The Role of Hybridization in Evolution|url=https://www.jstor.org/stable/985151|journal=Proceedings of the American Philosophical Society|volume=103|issue=2|pages=231–251|issn=0003-049X}}</ref><ref name=":4">{{Citation|last=Anderson|first=E.|last2=Stebbins|first2=G. L.|date=1954|title=Hybridization as an evolutionary stimulus|url=http://dx.doi.org/10.1111/j.1558-5646.1954.tb01504.x|journal=Evolution|volume=8|issue=4|pages=378–388|doi=10.1111/j.1558-5646.1954.tb01504.x|issn=0014-3820|via=}}</ref> Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals.<ref name=":0" /><ref name=":5">{{Citation|book|url=https://www.worldcat.org/oclc/960164734|title=Natural Hybridization and Evolution.|last=Arnold, Michael L.|date=1997|publisher=Oxford University Press|isbn=9780195356687|location=Cary|oclc=960164734}}</ref><ref name=":6">{{Citation|last=Mallet|first=James|last2=Besansky|first2=Nora|last3=Hahn|first3=Matthew W.|date=2016|title=How reticulated are species?|url=http://doi.wiley.com/10.1002/bies.201500149|journal=BioEssays|language=en|volume=38|issue=2|pages=140–149|doi=10.1002/bies.201500149|pmc=PMC4813508|pmid=26709836}}</ref> Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species.<ref name=":0" /> Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the ''[[w:Geospiza|Geospiza]]'' Galapagos finches,<ref name=":7">{{Citation|last=Lamichhaney|first=Sangeet|last2=Han|first2=Fan|last3=Webster|first3=Matthew T.|last4=Andersson|first4=Leif|last5=Grant|first5=B. Rosemary|last6=Grant|first6=Peter R.|date=2018|title=Rapid hybrid speciation in Darwin’s finches|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aao4593|journal=Science|language=en|volume=359|issue=6372|pages=224–228|doi=10.1126/science.aao4593|issn=0036-8075}}</ref> African [[w:cichlid|cichlid]] fishes,<ref name=":8">{{Citation|last=Meier|first=Joana I.|last2=Marques|first2=David A.|last3=Mwaiko|first3=Salome|last4=Wagner|first4=Catherine E.|last5=Excoffier|first5=Laurent|last6=Seehausen|first6=Ole|date=2017|title=Ancient hybridization fuels rapid cichlid fish adaptive radiations|url=http://www.nature.com/articles/ncomms14363|journal=Nature Communications|language=en|volume=8|issue=1|doi=10.1038/ncomms14363|issn=2041-1723|pmc=PMC5309898|pmid=28186104}}</ref> ''[[w:Heliconius|Heliconius]]'' butterflies<ref name=":9">{{Citation|last=Mavárez|first=Jesús|last2=Salazar|first2=Camilo A.|last3=Bermingham|first3=Eldredge|last4=Salcedo|first4=Christian|last5=Jiggins|first5=Chris D.|last6=Linares|first6=Mauricio|date=2006|title=Speciation by hybridization in Heliconius butterflies|url=http://www.nature.com/articles/nature04738|journal=Nature|language=en|volume=441|issue=7095|pages=868–871|doi=10.1038/nature04738|issn=0028-0836}}</ref><ref name=":10">{{Citation|last=Salazar|first=Camilo|last2=Baxter|first2=Simon W.|last3=Pardo-Diaz|first3=Carolina|last4=Wu|first4=Grace|last5=Surridge|first5=Alison|last6=Linares|first6=Mauricio|last7=Bermingham|first7=Eldredge|last8=Jiggins|first8=Chris D.|date=2010|editor-last=Walsh|editor-first=Bruce|title=Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies|url=https://dx.plos.org/10.1371/journal.pgen.1000930|journal=PLoS Genetics|language=en|volume=6|issue=4|pages=e1000930|doi=10.1371/journal.pgen.1000930|issn=1553-7404|pmc=PMC2861694|pmid=20442862}}</ref><ref name=":11">{{Citation|last=Melo|first=Maria C.|last2=Salazar|first2=Camilo|last3=Jiggins|first3=Chris D.|last4=Linares|first4=Mauricio|date=2009|title=Assortative mating preferences among hybrids offers a route to hybrid speciation|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00633.x|journal=Evolution|language=en|volume=63|issue=6|pages=1660–1665|doi=10.1111/j.1558-5646.2009.00633.x|via=}}</ref> and Hawaiian ''[[w:Madiinae|Madiinae]]'' tarweeds and silverswords.<ref name=":12">{{Citation|book|url=https://www.worldcat.org/oclc/52892451|title=Tarweeds & silverswords : evolution of the Madiinae (Asteraceae)|date=2003|publisher=Missouri Botanical Garden Press|others=Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D.|isbn=1930723202|location=St. Louis|oclc=52892451}}</ref> Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review). === Evolutionary outcomes of hybridization === There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species.<ref name=":13">{{Citation|last=Wolf|first=Diana E.|last2=Takebayashi|first2=Naoki|last3=Rieseberg|first3=Loren H.|date=2001|title=Predicting the Risk of Extinction through Hybridization|url=http://doi.wiley.com/10.1046/j.1523-1739.2001.0150041039.x|journal=Conservation Biology|language=en|volume=15|issue=4|pages=1039–1053|doi=10.1046/j.1523-1739.2001.0150041039.x|issn=0888-8892}}</ref><ref name=":14">{{Citation|last=Prentis|first=P. J.|last2=White|first2=E. M.|last3=Radford|first3=I. J.|last4=Lowe|first4=A. J.|last5=Clarke|first5=A. R.|date=2007|title=Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?|url=http://doi.wiley.com/10.1111/j.1469-8137.2007.02217.x|journal=New Phytologist|language=en|volume=176|issue=4|pages=902–912|doi=10.1111/j.1469-8137.2007.02217.x|issn=0028-646X}}</ref> This could potentially lead to [[w:reinforcement speciation|reinforcement]], selection to strengthen premating isolation<ref name=":15">{{Citation|last=Servedio|first=Maria R.|last2=Noor|first2=Mohamed A.F.|date=2003|title=The Role of Reinforcement in Speciation: Theory and Data|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.34.011802.132412|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=34|issue=1|pages=339–364|doi=10.1146/annurev.ecolsys.34.011802.132412|issn=1543-592X}}</ref> or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort.<ref name=":13" /> If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal<ref name=":16">{{Citation|last=Rhymer|first=Judith M.|last2=Simberloff|first2=Daniel|date=1996|title=EXTINCTION BY HYBRIDIZATION AND INTROGRESSION|url=http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.27.1.83|journal=Annual Review of Ecology and Systematics|language=en|volume=27|issue=1|pages=83–109|doi=10.1146/annurev.ecolsys.27.1.83|issn=0066-4162}}</ref><ref name=":17">{{Citation|last=Seehausen|first=Ole|date=2006|title=Conservation: Losing Biodiversity by Reverse Speciation|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982206014138|journal=Current Biology|language=en|volume=16|issue=9|pages=R334–R337|doi=10.1016/j.cub.2006.03.080}}</ref>; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa.<ref name=":18">{{Citation|last=Thompson|first=John D.|date=1994|title=Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.|url=http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x|journal=Journal of Evolutionary Biology|volume=7|issue=5|pages=631–634|doi=10.1046/j.1420-9101.1994.7050631.x|issn=1010-061X}}</ref> If hybrids are fertile, hybridization may contribute novel variation through rare hybrids [[w:backcrossing|backcrosssing]] with parental species. Such introgressive hybridization may enable neutral or selectively beneficial [[w:allele|allele]]s to be transferred across species boundaries even in species pairs that remain distinct despite occasional [[w:gene flow|gene flow]].<ref name=":19">{{Citation|last=The Heliconius Genome Consortium|date=2012|title=Butterfly genome reveals promiscuous exchange of mimicry adaptations among species|url=http://www.nature.com/articles/nature11041|journal=Nature|language=en|volume=487|issue=7405|pages=94–98|doi=10.1038/nature11041|issn=0028-0836|pmc=PMC3398145|pmid=22722851}}</ref><ref name=":20">{{Citation|last=Hanemaaijer|first=Mark J.|last2=Collier|first2=Travis C.|last3=Chang|first3=Allison|last4=Shott|first4=Chloe C.|last5=Houston|first5=Parker D.|last6=Schmidt|first6=Hanno|last7=Main|first7=Bradley J.|last8=Cornel|first8=Anthony J.|last9=Lee|first9=Yoosook|date=2018|title=The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population|url=http://doi.wiley.com/10.1111/mec.14947|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4978–4990|doi=10.1111/mec.14947}}</ref> Hybrid [[w:fitness biology|fitness]] may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including ''Drosophila'',<ref name=":21">{{Citation|book|url=https://www.worldcat.org/oclc/55078441|title=Speciation|last=Coyne|first=Jerry A.|last2=Orr|first2=H. Allen|date=2004|publisher=Sinauer Associates|others=|year=|isbn=0878930914|location=Sunderland|pages=|oclc=55078441}}</ref> birds<ref name=":22">{{Citation|last=Price|first=Trevor D.|last2=Bouvier|first2=Michelle M.|date=2002|title=The evolution of F1 postzygotic incompatibilities in birds|url=http://dx.doi.org/10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|journal=Evolution|volume=56|issue=10|pages=2083|doi=10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2|issn=0014-3820|via=}}</ref> and fish.<ref name=":23">{{Citation|last=Stelkens|first=Rike B.|last2=Young|first2=Kyle A.|last3=Seehausen|first3=Ole|date=2010|title=The accumulation of reproductive incompatibilities in African cichlid fish|url=http://doi.wiley.com/10.1111/j.1558-5646.2009.00849.x|journal=Evolution|language=en|volume=64|issue=3|pages=617–633|doi=10.1111/j.1558-5646.2009.00849.x|via=}}</ref> Hybrid fitness may also differ with cross direction,<ref name=":24">{{Citation|last=Rebernig|first=Carolin A.|last2=Lafon-Placette|first2=Clément|last3=Hatorangan|first3=Marcelinus R.|last4=Slotte|first4=Tanja|last5=Köhler|first5=Claudia|date=2015|editor-last=Bomblies|editor-first=Kirsten|title=Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm|url=https://dx.plos.org/10.1371/journal.pgen.1005295|journal=PLOS Genetics|language=en|volume=11|issue=6|pages=e1005295|doi=10.1371/journal.pgen.1005295|issn=1553-7404|pmc=PMC4472357|pmid=26086217}}</ref> between first generation and later generation hybrids,<ref name=":25">{{Citation|last=Pritchard|first=V. L.|last2=Knutson|first2=V. L.|last3=Lee|first3=M.|last4=Zieba|first4=J.|last5=Edmands|first5=S.|date=2013|title=Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus|url=http://doi.wiley.com/10.1111/jeb.12060|journal=Journal of Evolutionary Biology|language=en|volume=26|issue=2|pages=416–433|doi=10.1111/jeb.12060}}</ref> and among individuals within generations of the same cross-type.<ref name=":26">{{Citation|last=Rieseberg|first=Loren H|last2=Archer|first2=Margaret A|last3=Wayne|first3=Robert K|date=1999|title=Transgressive segregation, adaptation and speciation|url=http://dx.doi.org/10.1038/sj.hdy.6886170|journal=Heredity|volume=83|issue=4|pages=363–372|doi=10.1038/sj.hdy.6886170|issn=0018-067X}}</ref><ref name=":27">{{Citation|last=Burke|first=John M.|last2=Arnold|first2=Michael L.|date=2001|title=Genetics and the Fitness of Hybrids|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.35.102401.085719|journal=Annual Review of Genetics|language=en|volume=35|issue=1|pages=31–52|doi=10.1146/annurev.genet.35.102401.085719|issn=0066-4197}}</ref> In some cases hybrids may evolve into new hybrid species with [[w:reproductive isolation|reproductive isolation]] to both parent taxa.<ref name=":28">{{Citation|last=Mallet|first=James|date=2007|title=Hybrid speciation|url=http://www.nature.com/articles/nature05706|journal=Nature|language=en|volume=446|issue=7133|pages=279–283|doi=10.1038/nature05706|issn=0028-0836}}</ref><ref name=":29">{{Citation|last=Vallejo‐Marín|first=Mario|last2=Hiscock|first2=Simon J.|date=2016|title=Hybridization and hybrid speciation under global change|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.14004|journal=New Phytologist|language=en|volume=211|issue=4|pages=1170–1187|doi=10.1111/nph.14004|issn=0028-646X}}</ref> Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes. [[File:Fig1v3_Potential_outcomes_of_hybridization.jpg|thumb|Figure 1 Potential evolutionary outcomes of hybridization. While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.]] === Adaptive introgression === When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.<ref name=":0" />) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced,<ref name=":30">{{Citation|last=Barton|first=Nick|last2=Bengtsson|first2=Bengt Olle|date=1986|title=The barrier to genetic exchange between hybridising populations|url=http://www.nature.com/articles/hdy1986135|journal=Heredity|language=en|volume=57|issue=3|pages=357–376|doi=10.1038/hdy.1986.135|issn=0018-067X}}</ref><ref name=":31">{{Citation|last=Demon|first=Inez|last2=Haccou|first2=Patsy|last3=van den Bosch|first3=Frank|date=2007|title=Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci|url=https://linkinghub.elsevier.com/retrieve/pii/S0040580907000731|journal=Theoretical Population Biology|language=en|volume=72|issue=2|pages=292–304|doi=10.1016/j.tpb.2007.06.005}}</ref> or the adaptive [[w:loci|loci]] are tightly linked to deleterious ones.<ref name=":32">{{Citation|last=Uecker|first=Hildegard|last2=Setter|first2=Derek|last3=Hermisson|first3=Joachim|date=2015|title=Adaptive gene introgression after secondary contact|url=http://link.springer.com/10.1007/s00285-014-0802-y|journal=Journal of Mathematical Biology|language=en|volume=70|issue=7|pages=1523–1580|doi=10.1007/s00285-014-0802-y|issn=0303-6812|pmc=PMC4426140|pmid=24992884}}</ref> Examples of adaptive traits that have been transferred via introgression include an insecticide resistance gene that was transferred from ''[[w:Anopheles gambiae|Anopheles gambiae]]'' to ''[[w:Anopheles coluzzii|A. coluzzii]]''<ref name=":20" /> and the red warning wing colouration trait in ''Heliconius'' butterflies that is under natural selection from predators which has been introgressed from e.g. ''[[w:Heliconius melpomene|H. melpomene]]'' to ''[[w:Heliconius timareta|H. timareta]]''<ref name=":33">{{Citation|last=Pardo-Diaz|first=Carolina|last2=Salazar|first2=Camilo|last3=Baxter|first3=Simon W.|last4=Merot|first4=Claire|last5=Figueiredo-Ready|first5=Wilsea|last6=Joron|first6=Mathieu|last7=McMillan|first7=W. Owen|last8=Jiggins|first8=Chris D.|date=2012|editor-last=R. Kronforst|editor-first=Marcus|title=Adaptive Introgression across Species Boundaries in Heliconius Butterflies|url=http://dx.plos.org/10.1371/journal.pgen.1002752|journal=PLoS Genetics|language=en|volume=8|issue=6|pages=e1002752|doi=10.1371/journal.pgen.1002752|issn=1553-7404|pmc=PMC3380824|pmid=22737081}}</ref> and other ''Heliconius'' species.<ref name=":19" /> In the plant ''[[w:Arabidopsis arenosa|Arabidopsis arenosa]]'' some of the alleles conferring adaptation to drought and [[w:phytotoxicity|phytotoxic]] levels of metal have been introgressed from ''[[w:Arabidopsis lyrata|A. lyrata]]''.<ref name=":34">{{Citation|last=Arnold|first=Brian J.|last2=Lahner|first2=Brett|last3=DaCosta|first3=Jeffrey M.|last4=Weisman|first4=Caroline M.|last5=Hollister|first5=Jesse D.|last6=Salt|first6=David E.|last7=Bomblies|first7=Kirsten|last8=Yant|first8=Levi|date=2016|title=Borrowed alleles and convergence in serpentine adaptation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1600405113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=29|pages=8320–8325|doi=10.1073/pnas.1600405113|issn=0027-8424|pmc=PMC4961121|pmid=27357660}}</ref> Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans.<ref name=":35">{{Citation|last=Racimo|first=Fernando|last2=Sankararaman|first2=Sriram|last3=Nielsen|first3=Rasmus|last4=Huerta-Sánchez|first4=Emilia|date=2015|title=Evidence for archaic adaptive introgression in humans|url=http://www.nature.com/articles/nrg3936|journal=Nature Reviews Genetics|language=en|volume=16|issue=6|pages=359–371|doi=10.1038/nrg3936|issn=1471-0056|pmc=PMC4478293|pmid=25963373}}</ref> If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolated against other populations of the same species. Examples of this include ''Heliconius'' butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.<ref name=":36">{{Citation|last=Kronforst|first=M. R.|last2=Papa|first2=R.|date=2015|title=The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry|url=http://www.genetics.org/cgi/doi/10.1534/genetics.114.172387|journal=Genetics|language=en|volume=200|issue=1|pages=1–19|doi=10.1534/genetics.114.172387|issn=0016-6731|pmc=PMC4423356|pmid=25953905}}</ref>), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between ''H. t. florencia'' and ''H. t. linaresi'') and intermediate levels (e.g. ''H. c. galanthus''/''H. pachinus'') of divergence.<ref name=":37">{{Citation|last=Mérot|first=C.|last2=Salazar|first2=C.|last3=Merrill|first3=R. M.|last4=Jiggins|first4=C. D.|last5=Joron|first5=M.|date=2017|title=What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2017.0335|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=284|issue=1856|pages=20170335|doi=10.1098/rspb.2017.0335|issn=0962-8452|pmc=PMC5474069|pmid=28592669}}</ref> === What is a hybrid species? === One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation.<ref name=":0" /><ref name=":28" /> A hybrid species has an admixed genome and forms stable genetically distinct populations.<ref name=":28" /> Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation,<ref name=":38">{{Citation|last=Schumer|first=Molly|last2=Rosenthal|first2=Gil G.|last3=Andolfatto|first3=Peter|date=2014|title=How common is homoploid hybrid speciation|url=http://doi.wiley.com/10.1111/evo.12399|journal=Evolution|language=en|volume=68|issue=6|pages=1553–1560|doi=10.1111/evo.12399|via=}}</ref> but see<ref name=":39">{{Citation|last=Nieto Feliner|first=G|last2=Álvarez|first2=I|last3=Fuertes-Aguilar|first3=J|last4=Heuertz|first4=M|last5=Marques|first5=I|last6=Moharrek|first6=F|last7=Piñeiro|first7=R|last8=Riina|first8=R|last9=Rosselló|first9=J A|date=2017|title=Is homoploid hybrid speciation that rare? An empiricist’s view|url=http://www.nature.com/articles/hdy20177|journal=Heredity|language=en|volume=118|issue=6|pages=513–516|doi=10.1038/hdy.2017.7|issn=0018-067X|pmc=PMC5436029|pmid=28295029}}</ref>. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. ''[[w:Heliconius heurippa|Heliconius heurippa]]'',<ref name=":9" /><ref name=":10" /><ref name=":11" /> ''[[w:Passer italiae|Passer italiae]]'',<ref name=":27" /> and three ''[[w:Helianthus|Helianthus]]'' sunflower species<ref name=":40">{{Citation|last=Rieseberg|first=L. H.|date=2003|title=Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1086949|journal=Science|language=en|volume=301|issue=5637|pages=1211–1216|doi=10.1126/science.1086949|issn=0036-8075}}</ref> because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.<ref name=":38" /> Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f. <ref name=":41">{{Citation|book|url=https://www.worldcat.org/oclc/7552165|title=Plant speciation|last=Grant, Verne.|date=1981|publisher=Columbia University Press|isbn=0231051123|edition=2nd ed|location=New York|oclc=7552165}}</ref>). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation).<ref name=":28" /> A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.<ref name=":42">{{Citation|last=Schumer|first=Molly|last2=Xu|first2=Chenling|last3=Powell|first3=Daniel L.|last4=Durvasula|first4=Arun|last5=Skov|first5=Laurits|last6=Holland|first6=Chris|last7=Blazier|first7=John C.|last8=Sankararaman|first8=Sriram|last9=Andolfatto|first9=Peter|date=2018|title=Natural selection interacts with recombination to shape the evolution of hybrid genomes|url=http://www.sciencemag.org/lookup/doi/10.1126/science.aar3684|journal=Science|language=en|volume=360|issue=6389|pages=656–660|doi=10.1126/science.aar3684|issn=0036-8075|pmc=PMC6069607|pmid=29674434}}</ref><ref name=":43">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://dx.doi.org/10.1038/s41559-017-0437-7|journal=Nature Ecology & Evolution|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref>). === Homoploid and polyploid hybrid speciation === In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication ([[w:polyploidy|polyploidy]]) or not. Homoploid hybrid speciation [[w:hybrid speciation|Homoploid hybrid speciation]] is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2).<ref name=":0" /> The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by [[w:recombination (genetic)|recombination]].<ref name=":39" /><ref name=":40" /><ref name=":44">{{Citation|last=Buerkle|first=C. Alex|last2=Rieseberg|first2=Loren H.|date=2008|title=The rate of genome stabilization in homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1558-5646.2007.00267.x|journal=Evolution|language=en|volume=62|issue=2|pages=266–275|doi=10.1111/j.1558-5646.2007.00267.x|issn=0014-3820|pmc=PMC2442919|pmid=18039323|via=}}</ref><ref name=":45">{{Citation|last=Ungerer|first=M. C.|last2=Baird|first2=S. J. E.|last3=Pan|first3=J.|last4=Rieseberg|first4=L. H.|date=1998|title=Rapid hybrid speciation in wild sunflowers|url=http://www.pnas.org/cgi/doi/10.1073/pnas.95.20.11757|journal=Proceedings of the National Academy of Sciences|language=en|volume=95|issue=20|pages=11757–11762|doi=10.1073/pnas.95.20.11757|issn=0027-8424|pmc=PMC21713|pmid=9751738}}</ref><ref name=":46">{{Citation|last=Lai|first=Zhao|last2=Nakazato|first2=Takuya|last3=Salmaso|first3=Marzia|last4=Burke|first4=John M.|last5=Tang|first5=Shunxue|last6=Knapp|first6=Steven J.|last7=Rieseberg|first7=Loren H.|date=2005|title=Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species|url=http://www.genetics.org/lookup/doi/10.1534/genetics.105.042242|journal=Genetics|language=en|volume=171|issue=1|pages=291–303|doi=10.1534/genetics.105.042242|issn=0016-6731|pmc=PMC1456521|pmid=16183908}}</ref><ref name=":47">{{Citation|last=Elgvin|first=Tore O.|last2=Trier|first2=Cassandra N.|last3=Tørresen|first3=Ole K.|last4=Hagen|first4=Ingerid J.|last5=Lien|first5=Sigbjørn|last6=Nederbragt|first6=Alexander J.|last7=Ravinet|first7=Mark|last8=Jensen|first8=Henrik|last9=Sætre|first9=Glenn-Peter|date=2017|title=The genomic mosaicism of hybrid speciation|url=http://advances.sciencemag.org/lookup/doi/10.1126/sciadv.1602996|journal=Science Advances|language=en|volume=3|issue=6|pages=e1602996|doi=10.1126/sciadv.1602996|issn=2375-2548|pmc=PMC5470830|pmid=28630911}}</ref><ref name=":48">{{Citation|last=Runemark|first=Anna|last2=Trier|first2=Cassandra N.|last3=Eroukhmanoff|first3=Fabrice|last4=Hermansen|first4=Jo S.|last5=Matschiner|first5=Michael|last6=Ravinet|first6=Mark|last7=Elgvin|first7=Tore O.|last8=Sætre|first8=Glenn-Peter|date=2018|title=Variation and constraints in hybrid genome formation|url=http://www.nature.com/articles/s41559-017-0437-7|journal=Nature Ecology & Evolution|language=en|volume=2|issue=3|pages=549–556|doi=10.1038/s41559-017-0437-7|issn=2397-334X}}</ref> In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an [[w:allopolyploid|allopolyploid]] with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, [[w:autopolyploid|autopolyploid]]s are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals.<ref name=":49">{{Citation|last=Otto|first=Sarah P|last2=Whitton|first2=Jeannette|date=2000|title=Polyploid Incidence and Evolution|url=http://www.annualreviews.org/doi/10.1146/annurev.genet.34.1.401|journal=Annual Review of Genetics|language=en|volume=34|issue=1|pages=401–437|doi=10.1146/annurev.genet.34.1.401|issn=0066-4197}}</ref> Polyploid hybrids can be instantly isolated from their parental species through [[w:chromosome|chromosome]] number differences.<ref name=":49" /> [[File:Figure 2. Schematic representation of homoploid and allopolyploid hybrid speciation. Updated.svg|thumb|Figure 2. Schematic representation of homoploid and allopolyploid hybrid speciation. As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [48,49,85]. As allopolyploid example we use the monkeyflower ''Mimulus peregrinus'', an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).]] === Reproductive isolation against parent species === Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species.<ref name=":0" /><ref name=":38" /><ref name=":50">{{Citation|last=Abbott|first=Richard J|last2=Rieseberg|first2=Loren H|date=2012|editor-last=John Wiley & Sons, Ltd|title=Hybrid Speciation|url=http://doi.wiley.com/10.1002/9780470015902.a0001753.pub2|language=en|publisher=John Wiley & Sons, Ltd|doi=10.1002/9780470015902.a0001753.pub2|isbn=9780470016176|work=eLS}}</ref> Reproductive isolation against parent species is harder to achieve for homoploid hybrids where [[w:karyotype|karyotype]] differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental conditions (extrinsic or intrinsic barriers, respectively).<ref name=":51">{{Citation|last=Coyne|first=Jerry A|date=1989|title=Mutation rates in hybrids between sibling species of Drosophila|url=http://dx.doi.org/10.1038/hdy.1989.87|journal=Heredity|volume=63|issue=2|pages=155–162|doi=10.1038/hdy.1989.87|issn=0018-067X}}</ref> For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.<ref name=":29" /> Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier.<ref name=":52">{{Citation|last=Chase|first=Mark W|last2=Paun|first2=Ovidiu|last3=Fay|first3=Michael F|date=2010|title=Hybridization and speciation in angiosperms: arole for pollinator shifts?|url=http://jbiol.biomedcentral.com/articles/10.1186/jbiol231|journal=Journal of Biology|language=en|volume=9|issue=3|pages=21|doi=10.1186/jbiol231|issn=1475-4924}}</ref><ref name=":53">{{Citation|last=Grant|first=Verne|date=1949|title=Pollination systems as isolating mechanisms in angiosperms|url=http://doi.wiley.com/10.1111/j.1558-5646.1949.tb00007.x|journal=Evolution|language=en|volume=3|issue=1|pages=82–97|doi=10.1111/j.1558-5646.1949.tb00007.x|via=}}</ref><ref name=":54">{{Citation|last=Segraves|first=K. A.|last2=Thompson|first2=J. N.|date=1999|title=Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia|url=http://doi.wiley.com/10.1111/j.1558-5646.1999.tb04526.x|journal=Evolution|language=en|volume=53|issue=4|pages=1114–1127|doi=10.1111/j.1558-5646.1999.tb04526.x|via=}}</ref><ref name=":55">{{Citation|last=Moe|first=Annika M.|last2=Weiblen|first2=George D.|date=2012|title=Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)|url=http://doi.wiley.com/10.1111/j.1558-5646.2012.01727.x|journal=Evolution|language=en|volume=66|issue=12|pages=3710–3721|doi=10.1111/j.1558-5646.2012.01727.x|via=}}</ref> Strong extrinsic pre-zygotic has been shown to isolate the hybrid species ''Senecio eboracensis'' from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments.<ref name=":56">{{Citation|last=Lowe|first=A J|last2=Abbott|first2=R J|date=2004|title=Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)|url=http://www.nature.com/articles/6800432|journal=Heredity|language=en|volume=92|issue=5|pages=386–395|doi=10.1038/sj.hdy.6800432|issn=0018-067X}}</ref> Lowe & Abbott conclude that [[w:selfing|selfing]], timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation.<ref name=":56" /> Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids.<ref name=":57">{{Citation|last=Selz|first=O. M.|last2=Thommen|first2=R.|last3=Maan|first3=M. E.|last4=Seehausen|first4=O.|date=2014|title=Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish|url=http://doi.wiley.com/10.1111/jeb.12287|journal=Journal of Evolutionary Biology|language=en|volume=27|issue=2|pages=275–289|doi=10.1111/jeb.12287}}</ref> A similar pattern was found in ''Geospiza'' Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology,<ref name=":7" /> and hybrid ''Heliconius'' butterflies preferred the hybrid wing patterning over that of both parent species.<ref name=":11" /> Intrinsic differences in habitat use<ref name=":58">{{Citation|last=Schwarzbach|first=Andrea E.|last2=Donovan|first2=Lisa A.|last3=Rieseberg|first3=Loren H.|date=2001|title=Transgressive character expression in a hybrid sunflower species|url=http://dx.doi.org/10.2307/2657018|journal=American Journal of Botany|volume=88|issue=2|pages=270–277|doi=10.2307/2657018|issn=0002-9122}}</ref> or in phenology<ref name=":59">{{Citation|last=Mameli|first=Giulia|last2=López-Alvarado|first2=Javier|last3=Farris|first3=Emmanuele|last4=Susanna|first4=Alfonso|last5=Filigheddu|first5=Rossella|last6=Garcia-Jacas|first6=Núria|date=2014|title=The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea|url=https://academic.oup.com/botlinnean/article-lookup/doi/10.1111/boj.12177|journal=Botanical Journal of the Linnean Society|language=en|volume=175|issue=3|pages=453–467|doi=10.1111/boj.12177}}</ref> may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in ''[[w:Rhagoletis pomonella|Rhagoletis pomonella]]'' maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple <ref name=":60">{{Citation|last=Xie|first=X.|last2=Michel|first2=A. P.|last3=Schwarz|first3=D.|last4=Rull|first4=J.|last5=Velez|first5=S.|last6=Forbes|first6=A. A.|last7=Aluja|first7=M.|last8=Feder|first8=J. L.|date=2008|title=Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data|url=http://doi.wiley.com/10.1111/j.1420-9101.2008.01507.x|journal=Journal of Evolutionary Biology|language=en|volume=21|issue=3|pages=900–913|doi=10.1111/j.1420-9101.2008.01507.x|issn=1010-061X}}</ref><ref name=":61">{{Citation|last=Feder|first=J. L.|last2=Xie|first2=X.|last3=Rull|first3=J.|last4=Velez|first4=S.|last5=Forbes|first5=A.|last6=Leung|first6=B.|last7=Dambroski|first7=H.|last8=Filchak|first8=K. E.|last9=Aluja|first9=M.|date=2005|title=Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0502099102|journal=Proceedings of the National Academy of Sciences|language=en|volume=102|issue=Supplement 1|pages=6573–6580|doi=10.1073/pnas.0502099102|issn=0027-8424|pmc=PMC1131876|pmid=15851672}}</ref> and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In ''[[w:Xiphophorus|Xiphophorus]]'' swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions.<ref name=":62">{{Citation|last=Schumer|first=Molly|last2=Powell|first2=Daniel L.|last3=Delclós|first3=Pablo J.|last4=Squire|first4=Mattie|last5=Cui|first5=Rongfeng|last6=Andolfatto|first6=Peter|last7=Rosenthal|first7=Gil G.|date=2017|title=Assortative mating and persistent reproductive isolation in hybrids|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1711238114|journal=Proceedings of the National Academy of Sciences|language=en|volume=114|issue=41|pages=10936–10941|doi=10.1073/pnas.1711238114|issn=0027-8424|pmc=PMC5642718|pmid=28973863}}</ref> Hence, prezygotic reproductive barriers to gene flow may be environment dependent. Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on ''Helianthus'' sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences,<ref name=":46" /><ref name=":63">{{Citation|last=Rieseberg|first=L. H.|last2=Linder|first2=C. R.|last3=Seiler|first3=G. J.|date=1995|title=Chromosomal and genic barriers to introgression in Helianthus|url=https://www.ncbi.nlm.nih.gov/pubmed/8582621|journal=Genetics|volume=141|issue=3|pages=1163–1171|issn=0016-6731|pmc=1206838|pmid=8582621}}</ref> in combination with hybridization induced structural differences.<ref name=":46" /> Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow ''Passer italiae'' and its parent species.<ref name=":27" /> Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species,<ref name=":64">{{Citation|last=Comeault|first=Aaron A.|last2=Matute|first2=Daniel R.|date=2018|title=Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1809685115|journal=Proceedings of the National Academy of Sciences|language=en|volume=115|issue=39|pages=9761–9766|doi=10.1073/pnas.1809685115|issn=0027-8424|pmc=PMC6166845|pmid=30209213}}</ref> the population size of the hybrid species,<ref name=":65">{{Citation|last=Blanckaert|first=Alexandre|last2=Bank|first2=Claudia|date=2018|editor-last=Zhang|editor-first=Jianzhi|title=In search of the Goldilocks zone for hybrid speciation|url=https://dx.plos.org/10.1371/journal.pgen.1007613|journal=PLOS Genetics|language=en|volume=14|issue=9|pages=e1007613|doi=10.1371/journal.pgen.1007613|issn=1553-7404|pmc=PMC6145587|pmid=30192761}}</ref> the nature of selection acting on hybrids, and [[w:genetic linkage|linkage]] among incompatibilities to each other and to adaptive variants.<ref name=":66">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Rosenthal|first3=Gil G.|last4=Andolfatto|first4=Peter|date=2015|editor-last=Payseur|editor-first=Bret A.|title=Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities|url=http://dx.plos.org/10.1371/journal.pgen.1005041|journal=PLOS Genetics|language=en|volume=11|issue=3|pages=e1005041|doi=10.1371/journal.pgen.1005041|issn=1553-7404|pmc=PMC4359097|pmid=25768654}}</ref> Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through [[w:transgressive segregation|transgressive phenotype]]s,<ref name=":58" /> or through novel combinations of ecological traits from the parent species,<ref name=":67">{{Citation|last=Vereecken|first=Nicolas J|last2=Cozzolino|first2=Salvatore|last3=Schiestl|first3=Florian P|date=2010|title=Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids|url=http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-103|journal=BMC Evolutionary Biology|language=en|volume=10|issue=1|pages=103|doi=10.1186/1471-2148-10-103|issn=1471-2148|pmc=PMC2875231|pmid=20409296}}</ref> and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation. === Stabilization of hybrid genomes === Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, [[w:recombination (genetic)|recombination]] can destabilize the [[w:karyotype|karyotype]] and lead to aberrant [[w:meiosis|meiotic]] behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits <ref name=":68">{{Citation|last=Gaeta|first=Robert T.|last2=Chris Pires|first2=J.|date=2010|title=Homoeologous recombination in allopolyploids: the polyploid ratchet: Research review|url=http://doi.wiley.com/10.1111/j.1469-8137.2009.03089.x|journal=New Phytologist|language=en|volume=186|issue=1|pages=18–28|doi=10.1111/j.1469-8137.2009.03089.x}}</ref> as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization".<ref name=":44" /> Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids.<ref name=":69">{{Citation|last=Hvala|first=John A.|last2=Frayer|first2=Megan E.|last3=Payseur|first3=Bret A.|date=2018|title=Signatures of hybridization and speciation in genomic patterns of ancestry|url=http://doi.wiley.com/10.1111/evo.13509|journal=Evolution|language=en|volume=72|issue=8|pages=1540–1552|doi=10.1111/evo.13509|pmc=PMC6261709|pmid=29806154|via=}}</ref> The strength of the suppression is affected by the form of selection, [[w:dominance(genetics)|dominance]], and whether the locus was situated on an [[w:autosome|autosome]] or [[w:sex chromosome|sex chromosome]].<ref name=":69" /> The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid ''Helianthus'' sunflower species genomes,<ref name=":70">{{Citation|last=Rieseberg|first=L. H.|last2=Sinervo|first2=B.|last3=Linder|first3=C. R.|last4=Ungerer|first4=M. C.|last5=Arias|first5=D. M.|date=1996|title=Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids|url=http://dx.doi.org/10.1126/science.272.5262.741|journal=Science|volume=272|issue=5262|pages=741–745|doi=10.1126/science.272.5262.741|issn=0036-8075}}</ref> and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations.<ref name=":44" /> In ''Zymoseptoria'' fungi genomes were stabilized within ca. 400 generations,<ref name=":71">{{Citation|last=Stukenbrock|first=E. H.|last2=Christiansen|first2=F. B.|last3=Hansen|first3=T. T.|last4=Dutheil|first4=J. Y.|last5=Schierup|first5=M. H.|date=2012|title=Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1201403109|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=27|pages=10954–10959|doi=10.1073/pnas.1201403109|issn=0027-8424|pmc=PMC3390827|pmid=22711811}}</ref> whereas in hybrid ''Xiphophorus'' swordtail genomes<ref name=":72">{{Citation|last=Schumer|first=Molly|last2=Brandvain|first2=Yaniv|date=2016|title=Determining epistatic selection in admixed populations|url=http://doi.wiley.com/10.1111/mec.13641|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2577–2591|doi=10.1111/mec.13641}}</ref> genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization,<ref name=":73">{{Citation|last=Sankararaman|first=Sriram|last2=Mallick|first2=Swapan|last3=Dannemann|first3=Michael|last4=Prüfer|first4=Kay|last5=Kelso|first5=Janet|last6=Pääbo|first6=Svante|last7=Patterson|first7=Nick|last8=Reich|first8=David|date=2014|title=The genomic landscape of Neanderthal ancestry in present-day humans|url=http://www.nature.com/articles/nature12961|journal=Nature|language=en|volume=507|issue=7492|pages=354–357|doi=10.1038/nature12961|issn=0028-0836|pmc=PMC4072735|pmid=24476815}}</ref> and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.<ref name=":74">{{Citation|last=Eroukhmanoff|first=Fabrice|last2=Bailey|first2=Richard I.|last3=Elgvin|first3=Tore O.|last4=Hermansen|first4=Jo S.|last5=Runemark|first5=Anna R.|last6=Trier|first6=Cassandra N.|last7=Sætre|first7=Glenn-Peter|date=2017|title=Resolution of conflict between parental genomes in a hybrid species|url=http://biorxiv.org/lookup/doi/10.1101/102970|journal=bioRxiv|doi=10.1101/102970}}</ref> Given time, [[w:genetic drift|genetic drift]] will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations.<ref name=":44" /> Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not [[w:homozygous|homozygous]] for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative [[w:overdominance|overdominance]],<ref name=":75">{{Citation|last=Ohta|first=Tomoko|date=1971|title=Associative overdominance caused by linked detrimental mutations|url=http://dx.doi.org/10.1017/s0016672300012684|journal=Genetical Research|volume=18|issue=3|pages=277–286|doi=10.1017/s0016672300012684|issn=0016-6723}}</ref><ref name=":76">{{Citation|last=Zhao|first=Lei|last2=Charlesworth|first2=Brian|date=2016|title=Resolving the Conflict Between Associative Overdominance and Background Selection|url=http://www.genetics.org/lookup/doi/10.1534/genetics.116.188912|journal=Genetics|language=en|volume=203|issue=3|pages=1315–1334|doi=10.1534/genetics.116.188912|issn=0016-6731|pmc=PMC4937488|pmid=27182952}}</ref> may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions.<ref name=":77">{{Citation|last=Faria|first=Rui|last2=Johannesson|first2=Kerstin|last3=Butlin|first3=Roger K.|last4=Westram|first4=Anja M.|date=2019|title=Evolving Inversions|url=https://linkinghub.elsevier.com/retrieve/pii/S0169534718302866|journal=Trends in Ecology & Evolution|language=en|volume=34|issue=3|pages=239–248|doi=10.1016/j.tree.2018.12.005}}</ref> The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3).<ref name=":20" /><ref name=":78">{{Citation|last=Barton|first=Nicholas H.|date=2018|title=The consequences of an introgression event|url=http://doi.wiley.com/10.1111/mec.14950|journal=Molecular Ecology|language=en|volume=27|issue=24|pages=4973–4975|doi=10.1111/mec.14950|via=}}</ref><ref name=":79">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Salazar|first3=Camilo|last4=Jiggins|first4=Chris D.|date=2019|editor-last=Moyle|editor-first=Leonie|title=Recombination rate variation shapes barriers to introgression across butterfly genomes|url=http://dx.plos.org/10.1371/journal.pbio.2006288|journal=PLOS Biology|language=en|volume=17|issue=2|pages=e2006288|doi=10.1371/journal.pbio.2006288|issn=1545-7885|pmc=PMC6366726|pmid=30730876}}</ref> An insecticide resistance region was retained following a hybridization event in ''Anopheles coluzzi'',<ref name=":20" /> suggesting a role for selection in maintaining favourable introgressed regions. The local [[w:recombination frequency|recombination rate]] is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers ''[[w:Mimulus|Mimulus]]'',<ref name=":80">{{Citation|last=Brandvain|first=Yaniv|last2=Kenney|first2=Amanda M.|last3=Flagel|first3=Lex|last4=Coop|first4=Graham|last5=Sweigart|first5=Andrea L.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Speciation and Introgression between Mimulus nasutus and Mimulus guttatus|url=http://dx.plos.org/10.1371/journal.pgen.1004410|journal=PLoS Genetics|language=en|volume=10|issue=6|pages=e1004410|doi=10.1371/journal.pgen.1004410|issn=1553-7404|pmc=PMC4072524|pmid=24967630}}</ref> in ''[[w:Mus domesticus|Mus domesticus]]'' house mice,<ref name=":81">{{Citation|last=Janoušek|first=Václav|last2=Munclinger|first2=Pavel|last3=Wang|first3=Liuyang|last4=Teeter|first4=Katherine C.|last5=Tucker|first5=Priscilla K.|date=2015|title=Functional Organization of the Genome May Shape the Species Boundary in the House Mouse|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv011|journal=Molecular Biology and Evolution|language=en|volume=32|issue=5|pages=1208–1220|doi=10.1093/molbev/msv011|issn=1537-1719|pmc=PMC4408407|pmid=25631927}}</ref> in ''Heliconius'' butterflies<ref name=":79" /> and in ''Xiphophorus'' swordtail fish.<ref name=":42" /> Genome-wide incompatibilities have been identified in ''Xipophorous'' fish,<ref name=":82">{{Citation|last=Schumer|first=Molly|last2=Cui|first2=Rongfeng|last3=Powell|first3=Daniel L|last4=Dresner|first4=Rebecca|last5=Rosenthal|first5=Gil G|last6=Andolfatto|first6=Peter|date=2014|title=High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species|url=https://elifesciences.org/articles/02535|journal=eLife|language=en|volume=3|doi=10.7554/eLife.02535|issn=2050-084X|pmc=PMC4080447|pmid=24898754}}</ref> chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental ''Cyprinidae'' goldfish - carp hybrids<ref name=":83">{{Citation|last=Liu|first=Shaojun|last2=Luo|first2=Jing|last3=Chai|first3=Jing|last4=Ren|first4=Li|last5=Zhou|first5=Yi|last6=Huang|first6=Feng|last7=Liu|first7=Xiaochuan|last8=Chen|first8=Yubao|last9=Zhang|first9=Chun|date=2016|title=Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1512955113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=5|pages=1327–1332|doi=10.1073/pnas.1512955113|issn=0027-8424|pmc=PMC4747765|pmid=26768847}}</ref> and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows,<ref name=":48" /><ref name=":84">{{Citation|last=Trier|first=Cassandra N.|last2=Hermansen|first2=Jo S.|last3=Sætre|first3=Glenn-Peter|last4=Bailey|first4=Richard I.|date=2014|editor-last=Jiggins|editor-first=Chris D.|title=Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species|url=https://dx.plos.org/10.1371/journal.pgen.1004075|journal=PLoS Genetics|language=en|volume=10|issue=1|pages=e1004075|doi=10.1371/journal.pgen.1004075|issn=1553-7404|pmc=PMC3886922|pmid=24415954}}</ref> fungus<ref name=":85">{{Citation|last=Giordano|first=Luana|last2=Sillo|first2=Fabiano|last3=Garbelotto|first3=Matteo|last4=Gonthier|first4=Paolo|date=2018|title=Mitonuclear interactions may contribute to fitness of fungal hybrids|url=http://www.nature.com/articles/s41598-018-19922-w|journal=Scientific Reports|language=en|volume=8|issue=1|doi=10.1038/s41598-018-19922-w|issn=2045-2322|pmc=PMC5786003|pmid=29374209}}</ref> and cyto-nuclear incompatibilities in ''Mimulus'' plants.<ref name=":86">{{Citation|last=Case|first=Andrea L.|last2=Finseth|first2=Findley R.|last3=Barr|first3=Camille M.|last4=Fishman|first4=Lila|date=2016|title=Selfish evolution of cytonuclear hybrid incompatibility in Mimulus|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2016.1493|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=283|issue=1838|pages=20161493|doi=10.1098/rspb.2016.1493|issn=0962-8452|pmc=PMC5031664|pmid=27629037}}</ref> Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair<ref name=":48" /><ref name=":83" /><ref name=":87">{{Citation|last=David|first=Wendi M.|last2=Mitchell|first2=David L.|last3=Walter|first3=Ronald B.|date=2004|title=DNA repair in hybrid fish of the genus Xiphophorus|url=https://linkinghub.elsevier.com/retrieve/pii/S1532045604001322|journal=Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology|language=en|volume=138|issue=3|pages=301–309|doi=10.1016/j.cca.2004.07.006}}</ref> and genes involved in mutagenesis and cancer related pathways<ref name=":83" /> may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.<ref name=":42" /><ref name=":72" /><ref name=":78" /> [[File:Figure 3. The process of genome stabilization during hybrid speciation and introgression.svg|thumb|Figure3. The process of genome stabilization during hybrid speciation and introgression. Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxa that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.]] === Altered genome properties in hybrid taxa === The hybrid origin may affect genome structure and properties. It has been shown to increase [[w:mutation rate|mutation rate]]s,<ref name=":51" /><ref name=":88">{{Citation|last=Ávila|first=Victoria|last2=Chavarrías|first2=David|last3=Sánchez|first3=Enrique|last4=Manrique|first4=Antonio|last5=López-Fanjul|first5=Carlos|last6=García-Dorado|first6=Aurora|date=2006|title=Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster|url=http://www.genetics.org/lookup/doi/10.1534/genetics.106.056200|journal=Genetics|language=en|volume=173|issue=1|pages=267–277|doi=10.1534/genetics.106.056200|issn=0016-6731|pmc=PMC1461422|pmid=16547099}}</ref><ref name=":89">{{Citation|last=Bashir|first=Tufail|last2=Sailer|first2=Christian|last3=Gerber|first3=Florian|last4=Loganathan|first4=Nitin|last5=Bhoopalan|first5=Hemadev|last6=Eichenberger|first6=Christof|last7=Grossniklaus|first7=Ueli|last8=Baskar|first8=Ramamurthy|date=2014|title=Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis|url=http://www.plantphysiol.org/lookup/doi/10.1104/pp.114.238451|journal=Plant Physiology|language=en|volume=165|issue=1|pages=424–437|doi=10.1104/pp.114.238451|issn=0032-0889|pmc=PMC4012600|pmid=24664208}}</ref> to activate transposable elements,<ref name=":90">{{Citation|last=Dennenmoser|first=Stefan|last2=Sedlazeck|first2=Fritz J.|last3=Iwaszkiewicz|first3=Elzbieta|last4=Li|first4=Xiang-Yi|last5=Altmüller|first5=Janine|last6=Nolte|first6=Arne W.|date=2017|title=Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin|url=http://doi.wiley.com/10.1111/mec.14134|journal=Molecular Ecology|language=en|volume=26|issue=18|pages=4712–4724|doi=10.1111/mec.14134|pmc=PMC5638112|pmid=28390096}}</ref><ref name=":91">{{Citation|last=Dion-Côté|first=Anne-Marie|last2=Renaut|first2=Sébastien|last3=Normandeau|first3=Eric|last4=Bernatchez|first4=Louis|date=2014|title=RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu069|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1188–1199|doi=10.1093/molbev/msu069|issn=1537-1719}}</ref><ref name=":92">{{Citation|last=Senerchia|first=Natacha|last2=Felber|first2=François|last3=Parisod|first3=Christian|date=2015|title=Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2014.2874|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=282|issue=1804|pages=20142874|doi=10.1098/rspb.2014.2874|issn=0962-8452|pmc=PMC4375867|pmid=25716787|via=}}</ref> and to induce [[w:chromosomal rearrangements|chromosomal rearrangements]].<ref name=":93">{{Citation|last=Ostberg|first=Carl O|last2=Hauser|first2=Lorenz|last3=Pritchard|first3=Victoria L|last4=Garza|first4=John C|last5=Naish|first5=Kerry A|date=2013|title=Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-570|journal=BMC Genomics|language=en|volume=14|issue=1|pages=570|doi=10.1186/1471-2164-14-570|issn=1471-2164|pmc=PMC3765842|pmid=23968234}}</ref><ref name=":94">{{Citation|last=Hirai|first=Hirohisa|last2=Hirai|first2=Yuriko|last3=Morimoto|first3=Mayumi|last4=Kaneko|first4=Akihisa|last5=Kamanaka|first5=Yoshiro|last6=Koga|first6=Akihiko|date=2017|title=Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates|url=https://academic.oup.com/gbe/article/9/4/945/3078090|journal=Genome Biology and Evolution|language=en|volume=9|issue=4|pages=945–955|doi=10.1093/gbe/evx058|issn=1759-6653|pmc=PMC5388293|pmid=28369492}}</ref> Increased [[w:transposon|transposon]] activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption.<ref name=":95">{{Citation|last=Barkan|first=A.|last2=Martienssen|first2=R. A.|date=1991|title=Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.|url=http://www.pnas.org/cgi/doi/10.1073/pnas.88.8.3502|journal=Proceedings of the National Academy of Sciences|language=en|volume=88|issue=8|pages=3502–3506|doi=10.1073/pnas.88.8.3502|issn=0027-8424}}</ref><ref name=":96">{{Citation|last=Raizada|first=Manish N.|last2=Benito|first2=Maria-Ines|last3=Walbot|first3=Virginia|date=2008|title=The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern|url=http://doi.wiley.com/10.1111/j.1365-313X.2001.00939.x|journal=The Plant Journal|language=en|volume=25|issue=1|pages=79–91|doi=10.1111/j.1365-313X.2001.00939.x}}</ref> For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in ''Nicotiana''.<ref name=":97">{{Citation|last=Lim|first=Kar Yoong|last2=Matyasek|first2=Roman|last3=Kovarik|first3=Ales|last4=Leitch|first4=Andrew R.|date=2004|title=Genome evolution in allotetraploid Nicotiana|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00344.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=599–606|doi=10.1111/j.1095-8312.2004.00344.x|via=}}</ref> Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease.<ref name=":98">{{Citation|last=Baack|first=Eric J.|last2=Whitney|first2=Kenneth D.|last3=Rieseberg|first3=Loren H.|date=2005|title=Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species|url=http://doi.wiley.com/10.1111/j.1469-8137.2005.01433.x|journal=New Phytologist|language=en|volume=167|issue=2|pages=623–630|doi=10.1111/j.1469-8137.2005.01433.x}}</ref> Both increases and decreases were found in the ''Nicotiana'' genus, and were not related to the age since hybridization.<ref name=":99">{{Citation|last=Leitch|first=I. J.|last2=Hanson|first2=L.|last3=Lim|first3=K. Y.|last4=Kovarik|first4=A.|last5=Chase|first5=M. W.|last6=Clarkson|first6=J. J.|last7=Leitch|first7=A. R.|date=2008|title=The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)|url=https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mcm326|journal=Annals of Botany|language=en|volume=101|issue=6|pages=805–814|doi=10.1093/aob/mcm326|issn=0305-7364|pmc=PMC2710205|pmid=18222910}}</ref> Following genome duplication in allopolyploids, the genome goes through [[w:diploidization|diploidization]], which is a process in which the genome is rearranged to act as a meiotic diploid. <ref name=":100">{{Citation|last=Wolfe|first=Kenneth H.|date=2001|title=Yesterday's polyploids and the mystery of diploidization|url=http://www.nature.com/articles/35072009|journal=Nature Reviews Genetics|language=en|volume=2|issue=5|pages=333–341|doi=10.1038/35072009|issn=1471-0056}}</ref><ref name=":101">{{Citation|last=Freeling|first=Michael|last2=Scanlon|first2=Michael J|last3=Fowler|first3=John E|date=2015|title=Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences|url=https://linkinghub.elsevier.com/retrieve/pii/S0959437X15001173|journal=Current Opinion in Genetics & Development|language=en|volume=35|pages=110–118|doi=10.1016/j.gde.2015.11.002}}</ref> After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes.<ref name=":101" /><ref name=":102">{{Citation|last=Sankoff|first=David|last2=Zheng|first2=Chunfang|last3=Zhu|first3=Qian|date=2010|title=The collapse of gene complement following whole genome duplication|url=http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-313|journal=BMC Genomics|language=en|volume=11|issue=1|pages=313|doi=10.1186/1471-2164-11-313|issn=1471-2164|pmc=PMC2896955|pmid=20482863}}</ref> In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.<ref name=":102" /> A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between [[w:homologous chromosomes|homologous chromosomes]] are biased in favour of this subgenome, as compared with the other subgenomes.<ref name=":103">{{Citation|last=Edger|first=Patrick P.|last2=Poorten|first2=Thomas J.|last3=VanBuren|first3=Robert|last4=Hardigan|first4=Michael A.|last5=Colle|first5=Marivi|last6=McKain|first6=Michael R.|last7=Smith|first7=Ronald D.|last8=Teresi|first8=Scott J.|last9=Nelson|first9=Andrew D. L.|date=2019|title=Origin and evolution of the octoploid strawberry genome|url=http://www.nature.com/articles/s41588-019-0356-4|journal=Nature Genetics|language=en|volume=51|issue=3|pages=541–547|doi=10.1038/s41588-019-0356-4|issn=1061-4036}}</ref> This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent.<ref name=":103" /> A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome.<ref name=":101" /><ref name=":104">{{Citation|last=Edger|first=Patrick P.|last2=Smith|first2=Ronald|last3=McKain|first3=Michael R.|last4=Cooley|first4=Arielle M.|last5=Vallejo-Marin|first5=Mario|last6=Yuan|first6=Yaowu|last7=Bewick|first7=Adam J.|last8=Ji|first8=Lexiang|last9=Platts|first9=Adrian E.|date=2017|title=Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower|url=http://www.plantcell.org/lookup/doi/10.1105/tpc.17.00010|journal=The Plant Cell|language=en|volume=29|issue=9|pages=2150–2167|doi=10.1105/tpc.17.00010|issn=1040-4651|pmc=PMC5635986|pmid=28814644}}</ref> Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.<ref name=":104" /> In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species.<ref name=":105">{{Citation|last=Xu|first=Chunming|last2=Bai|first2=Yan|last3=Lin|first3=Xiuyun|last4=Zhao|first4=Na|last5=Hu|first5=Lanjuan|last6=Gong|first6=Zhiyun|last7=Wendel|first7=Jonathan F.|last8=Liu|first8=Bao|date=2014|title=Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu085|journal=Molecular Biology and Evolution|language=en|volume=31|issue=5|pages=1066–1076|doi=10.1093/molbev/msu085|issn=1537-1719|pmc=PMC3995341|pmid=24577842}}</ref><ref name=":106">{{Citation|last=Renaut|first=S.|last2=Nolte|first2=A.W.|last3=Bernatchez|first3=L.|date=2009|title=Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msp017|journal=Molecular Biology and Evolution|language=en|volume=26|issue=4|pages=925–936|doi=10.1093/molbev/msp017|issn=1537-1719}}</ref> Studies of synthetic and natural allopolyploids of ''Tragopogon miscellus'' show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations.<ref name=":107">{{Citation|last=Buggs|first=Richard J.A.|last2=Zhang|first2=Linjing|last3=Miles|first3=Nicholas|last4=Tate|first4=Jennifer A.|last5=Gao|first5=Lu|last6=Wei|first6=Wu|last7=Schnable|first7=Patrick S.|last8=Barbazuk|first8=W. Brad|last9=Soltis|first9=Pamela S.|date=2011|title=Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant|url=https://linkinghub.elsevier.com/retrieve/pii/S0960982211002077|journal=Current Biology|language=en|volume=21|issue=7|pages=551–556|doi=10.1016/j.cub.2011.02.016}}</ref> While expression variation in [[w:miRNA|miRNA]]s alters gene expression and affects growth in the natural allopolyploid ''Arabidopsis suecica'' and experimental lineages, inheritance of [[w:siRNA|siRNA]]s is stable and maintains chromatin and genome stability,<ref name=":108">{{Citation|last=Ha|first=M.|last2=Lu|first2=J.|last3=Tian|first3=L.|last4=Ramachandran|first4=V.|last5=Kasschau|first5=K. D.|last6=Chapman|first6=E. J.|last7=Carrington|first7=J. C.|last8=Chen|first8=X.|last9=Wang|first9=X.-J.|date=2009|title=Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids|url=http://www.pnas.org/cgi/doi/10.1073/pnas.0907003106|journal=Proceedings of the National Academy of Sciences|language=en|volume=106|issue=42|pages=17835–17840|doi=10.1073/pnas.0907003106|issn=0027-8424|pmc=PMC2757398|pmid=19805056}}</ref> potentially buffering against a transcriptomic shock. === What factors influence the likelihood of the formation of persistent hybrid genomes? === Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages. Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species.<ref name=":109">{{Citation|last=Mallet|first=James|date=2005|title=Hybridization as an invasion of the genome|url=https://linkinghub.elsevier.com/retrieve/pii/S016953470500039X|journal=Trends in Ecology & Evolution|language=en|volume=20|issue=5|pages=229–237|doi=10.1016/j.tree.2005.02.010}}</ref> Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes.<ref name=":110">{{Citation|last=Charlesworth|first=Deborah|date=2016|title=Plant Sex Chromosomes|url=http://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111911|journal=Annual Review of Plant Biology|language=en|volume=67|issue=1|pages=397–420|doi=10.1146/annurev-arplant-043015-111911|issn=1543-5008}}</ref> The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation,<ref name=":111">{{Citation|last=Rieseberg|first=Loren H.|date=2001|title=Chromosomal rearrangements and speciation|url=http://dx.doi.org/10.1016/s0169-5347(01)02187-5|journal=Trends in Ecology & Evolution|volume=16|issue=7|pages=351–358|doi=10.1016/s0169-5347(01)02187-5|issn=0169-5347}}</ref><ref name=":112">{{Citation|last=Levin|first=Donald A.|date=2012|title=The long wait for hybrid sterility in flowering plants|url=http://doi.wiley.com/10.1111/j.1469-8137.2012.04309.x|journal=New Phytologist|language=en|volume=196|issue=3|pages=666–670|doi=10.1111/j.1469-8137.2012.04309.x}}</ref> and may hence enable hybridization between phylogenetically more distant taxa. [[w:Haldane's rule|Haldane's rule]]<ref name=":113">{{Citation|last=Haldane|first=J. B. S.|date=1922|title=Sex ratio and unisexual sterility in hybrid animals|url=http://link.springer.com/10.1007/BF02983075|journal=Journal of Genetics|language=en|volume=12|issue=2|pages=101–109|doi=10.1007/BF02983075|issn=0022-1333}}</ref> states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of [[w:heterogametic sex|heterogametic]] hybrids.<ref name=":21" /> These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to [[w:hemozygosity|hemizygous]] expression.<ref name=":114">{{Citation|last=Turelli|first=M.|last2=Orr|first2=H. A.|date=1995|title=The dominance theory of Haldane's rule|url=https://www.ncbi.nlm.nih.gov/pubmed/7635302|journal=Genetics|volume=140|issue=1|pages=389–402|issn=0016-6731|pmc=1206564|pmid=7635302}}</ref> In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see <ref name=":115">{{Citation|last=Runemark|first=Anna|last2=Eroukhmanoff|first2=Fabrice|last3=Nava-Bolaños|first3=Angela|last4=Hermansen|first4=Jo S.|last5=Meier|first5=Joana I.|date=2018|title=Hybridization, sex-specific genomic architecture and local adaptation|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0419|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1757|pages=20170419|doi=10.1098/rstb.2017.0419|issn=0962-8436|pmc=PMC6125728|pmid=30150218}}</ref> for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems.<ref name=":116">{{Citation|last=Payseur|first=Bret A.|last2=Rieseberg|first2=Loren H.|date=2016|title=A genomic perspective on hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.13557|journal=Molecular Ecology|language=en|volume=25|issue=11|pages=2337–2360|doi=10.1111/mec.13557|pmc=PMC4915564|pmid=26836441}}</ref> This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes,<ref name=":117">{{Citation|book|url=https://www.worldcat.org/oclc/37030646|title=Genetics and analysis of quantitative traits|last=Lynch|first=Michael|date=1998|publisher=Sinauer|others=Walsh, Bruce, 1957-|year=|isbn=0878934812|location=Sunderland, Mass.|pages=|oclc=37030646}}</ref> the elevated frequency of loci involved in reproductive isolation<ref name=":118">{{Citation|last=Masly|first=John P|last2=Presgraves|first2=Daven C|date=2007|editor-last=Barton|editor-first=Nick H|title=High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila|url=https://dx.plos.org/10.1371/journal.pbio.0050243|journal=PLoS Biology|language=en|volume=5|issue=9|pages=e243|doi=10.1371/journal.pbio.0050243|issn=1545-7885|pmc=PMC1971125|pmid=17850182}}</ref> and/or the heightened conflict on sex chromosomes.<ref name=":119">{{Citation|last=Mank|first=J. E.|last2=Hosken|first2=D. J.|last3=Wedell|first3=N.|date=2014|title=Conflict on the Sex Chromosomes: Cause, Effect, and Complexity|url=http://cshperspectives.cshlp.org/lookup/doi/10.1101/cshperspect.a017715|journal=Cold Spring Harbor Perspectives in Biology|language=en|volume=6|issue=12|pages=a017715–a017715|doi=10.1101/cshperspect.a017715|issn=1943-0264|pmc=PMC4292157|pmid=25280765}}</ref> Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows<ref name=":48" /> is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes. There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades.<ref name=":3" /> In plants, high rates of [[w:selfing|selfing]] in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer.<ref name=":120">{{Citation|last=Brys|first=Rein|last2=Broeck|first2=An Vanden|last3=Mergeay|first3=Joachim|last4=Jacquemyn|first4=Hans|date=2014|title=The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology|url=http://doi.wiley.com/10.1111/evo.12345|journal=Evolution|language=en|volume=68|issue=5|pages=1281–1293|doi=10.1111/evo.12345|via=}}</ref><ref name=":121">{{Citation|last=Widmer|first=A|last2=Lexer|first2=C|last3=Cozzolino|first3=S|date=2009|title=Evolution of reproductive isolation in plants|url=http://www.nature.com/articles/hdy200869|journal=Heredity|language=en|volume=102|issue=1|pages=31–38|doi=10.1038/hdy.2008.69|issn=0018-067X}}</ref> In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae<ref name=":122">{{Citation|last=Schardl|first=C. L.|last2=Craven|first2=K. D.|date=2003|title=Interspecific hybridization in plant-associated fungi and oomycetes: a review|url=http://dx.doi.org/10.1046/j.1365-294x.2003.01965.x|journal=Molecular Ecology|volume=12|issue=11|pages=2861–2873|doi=10.1046/j.1365-294x.2003.01965.x|issn=0962-1083}}</ref> in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent [[w:parasexual cycle|parasexual]] mating with mitotic crossover may generate recombined hybrid cells.<ref name=":122" /> For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. [[w:polyploidisation|Polyploidisation]] and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare [[w:karyotype|cytotype]]s are at a reproductive disadvantage due to inter-cytotype mating.<ref name=":123">{{Citation|last=Levin|first=Donald A.|date=1975|title=Minority Cytotype Exclusion in Local Plant Populations|url=http://doi.wiley.com/10.2307/1218997|journal=Taxon|language=en|volume=24|issue=1|pages=35–43|doi=10.2307/1218997|via=}}</ref> Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study,<ref name=":124">{{Citation|last=McCarthy|first=Eugene M|last2=Asmussen|first2=Marjorie A|last3=Anderson|first3=Wyatt W|date=1995|title=A theoretical assessment of recombinational speciation|url=http://www.nature.com/articles/hdy199571|journal=Heredity|language=en|volume=74|issue=5|pages=502–509|doi=10.1038/hdy.1995.71|issn=0018-067X}}</ref> and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as ''Epichloe'' fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species.<ref name=":125">{{Citation|last=Charlton|first=Nikki D.|last2=Craven|first2=Kelly D.|last3=Afkhami|first3=Michelle E.|last4=Hall|first4=Bradley A.|last5=Ghimire|first5=Sita R.|last6=Young|first6=Carolyn A.|date=2014|title=Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes|url=https://academic.oup.com/femsec/article-lookup/doi/10.1111/1574-6941.12393|journal=FEMS Microbiology Ecology|language=en|volume=90|issue=1|pages=276–289|doi=10.1111/1574-6941.12393}}</ref> Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, ''Cobitis'',<ref name=":126">{{Citation|last=Janko|first=Karel|last2=Pačes|first2=Jan|last3=Wilkinson-Herbots|first3=Hilde|last4=Costa|first4=Rui J.|last5=Roslein|first5=Jan|last6=Drozd|first6=Pavel|last7=Iakovenko|first7=Nataliia|last8=Rídl|first8=Jakub|last9=Hroudová|first9=Miluše|date=2018|title=Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation|url=http://doi.wiley.com/10.1111/mec.14377|journal=Molecular Ecology|language=en|volume=27|issue=1|pages=248–263|doi=10.1111/mec.14377}}</ref> and most if not all asexual vertebrate species are of hybrid origin.<ref name=":127">{{Citation|last=Neaves|first=William B.|last2=Baumann|first2=Peter|date=2011|title=Unisexual reproduction among vertebrates|url=https://linkinghub.elsevier.com/retrieve/pii/S0168952510002295|journal=Trends in Genetics|language=en|volume=27|issue=3|pages=81–88|doi=10.1016/j.tig.2010.12.002}}</ref> Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants,<ref name=":128">{{Citation|last=Brochmann|first=C.|last2=Brysting|first2=A. K.|last3=Alsos|first3=I. G.|last4=Borgen|first4=L.|last5=Grundt|first5=H. H.|last6=Scheen|first6=A.-C.|last7=Elven|first7=R.|date=2004|title=Polyploidy in arctic plants|url=https://academic.oup.com/biolinnean/article-lookup/doi/10.1111/j.1095-8312.2004.00337.x|journal=Biological Journal of the Linnean Society|language=en|volume=82|issue=4|pages=521–536|doi=10.1111/j.1095-8312.2004.00337.x|via=}}</ref> suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation. For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an ''Anopheles gambiae'' resistance allele into ''A. coluzzi'' malaria mosquitoes.<ref name=":129">{{Citation|last=Norris|first=Laura C.|last2=Main|first2=Bradley J.|last3=Lee|first3=Yoosook|last4=Collier|first4=Travis C.|last5=Fofana|first5=Abdrahamane|last6=Cornel|first6=Anthony J.|last7=Lanzaro|first7=Gregory C.|date=2015|title=Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1418892112|journal=Proceedings of the National Academy of Sciences|language=en|volume=112|issue=3|pages=815–820|doi=10.1073/pnas.1418892112|issn=0027-8424|pmc=PMC4311837|pmid=25561525}}</ref> In ''Heliconius'' butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies.<ref name=":33" /> Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against. === What genes and genomic regions are affected by hybridization? === Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into [[w:secondary contact|secondary contact]]. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes.<ref name=":130">{{Citation|last=Marques|first=David A.|last2=Meier|first2=Joana I.|last3=Seehausen|first3=Ole|date=2019|title=A Combinatorial View on Speciation and Adaptive Radiation|url=http://dx.doi.org/10.1016/j.tree.2019.02.008|journal=Trends in Ecology & Evolution|volume=34|issue=6|pages=531–544|doi=10.1016/j.tree.2019.02.008|issn=0169-5347}}</ref> Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness<ref name=":131">{{Citation|last=Maheshwari|first=Shamoni|last2=Barbash|first2=Daniel A.|date=2011|title=The Genetics of Hybrid Incompatibilities|url=http://www.annualreviews.org/doi/10.1146/annurev-genet-110410-132514|journal=Annual Review of Genetics|language=en|volume=45|issue=1|pages=331–355|doi=10.1146/annurev-genet-110410-132514|issn=0066-4197}}</ref> but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above.<ref name=":130" /> An intermediate genetic distance may thus be most condusive to hybrid speciation.<ref name=":130" /> Experimental lab crosses support this hypothesis.<ref name=":64" /> The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome.<ref name=":132">{{Citation|last=Buggs|first=R J A|last2=Doust|first2=A N|last3=Tate|first3=J A|last4=Koh|first4=J|last5=Soltis|first5=K|last6=Feltus|first6=F A|last7=Paterson|first7=A H|last8=Soltis|first8=P S|last9=Soltis|first9=D E|date=2009|title=Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids|url=http://www.nature.com/articles/hdy200924|journal=Heredity|language=en|volume=103|issue=1|pages=73–81|doi=10.1038/hdy.2009.24|issn=0018-067X}}</ref> Relatively equal parental contributions are also found in some homoploid hybrid species<ref name=":47" /> but in other cases they are highly unequal such as in some ''Heliconius'' species.<ref name=":133">{{Citation|last=Jiggins|first=Chris D|last2=Salazar|first2=Camilo|last3=Linares|first3=Mauricio|last4=Mavarez|first4=Jesus|date=2008|title=Hybrid trait speciation and Heliconius butterflies|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2008.0065|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=363|issue=1506|pages=3047–3054|doi=10.1098/rstb.2008.0065|issn=0962-8436|pmc=PMC2607310|pmid=18579480}}</ref> The majority ancestry may even be that from the donor of introgressed material, as was shown for ''Anopheles gambiae'' mosquitoes.<ref name=":134">{{Citation|last=Fontaine|first=Michael C.|last2=Pease|first2=James B.|last3=Steele|first3=Aaron|last4=Waterhouse|first4=Robert M.|last5=Neafsey|first5=Daniel E.|last6=Sharakhov|first6=Igor V.|last7=Jiang|first7=Xiaofang|last8=Hall|first8=Andrew B.|last9=Catteruccia|first9=Flaminia|date=2015|title=Extensive introgression in a malaria vector species complex revealed by phylogenomics|url=http://www.sciencemag.org/lookup/doi/10.1126/science.1258524|journal=Science|language=en|volume=347|issue=6217|pages=1258524|doi=10.1126/science.1258524|issn=0036-8075|pmc=PMC4380269|pmid=25431491}}</ref> Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.<ref name=":42" /><ref name=":43" /> Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance<ref name=":20" /> and introgression of a divergent, inverted chromosomal segment has resulted in a ”[[w:super gene|super gene]]” that encodes mimicry polymorphism in the butterfly ''Heliconius numata''.<ref name=":135">{{Citation|last=Jay|first=Paul|last2=Whibley|first2=Annabel|last3=Frézal|first3=Lise|last4=Rodríguez de Cara|first4=María Ángeles|last5=Nowell|first5=Reuben W.|last6=Mallet|first6=James|last7=Dasmahapatra|first7=Kanchon K.|last8=Joron|first8=Mathieu|date=2018|title=Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion|url=https://linkinghub.elsevier.com/retrieve/pii/S096098221830544X|journal=Current Biology|language=en|volume=28|issue=11|pages=1839–1845.e3|doi=10.1016/j.cub.2018.04.072}}</ref> These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci.<ref name=":136">{{Citation|last=Yeaman|first=S.|date=2013|title=Genomic rearrangements and the evolution of clusters of locally adaptive loci|url=http://www.pnas.org/cgi/doi/10.1073/pnas.1219381110|journal=Proceedings of the National Academy of Sciences|language=en|volume=110|issue=19|pages=E1743–E1751|doi=10.1073/pnas.1219381110|issn=0027-8424|pmc=PMC3651494|pmid=23610436}}</ref> Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries,<ref name=":18" /><ref name=":137">{{Citation|last=Wu|first=Chung-I|date=2001|title=The genic view of the process of speciation: Genic view of the process of speciation|url=http://doi.wiley.com/10.1046/j.1420-9101.2001.00335.x|journal=Journal of Evolutionary Biology|language=en|volume=14|issue=6|pages=851–865|doi=10.1046/j.1420-9101.2001.00335.x}}</ref><ref name=":138">{{Citation|last=Harrison|first=Richard G.|last2=Larson|first2=Erica L.|date=2014|title=Hybridization, Introgression, and the Nature of Species Boundaries|url=https://academic.oup.com/jhered/jhered/article/2961884/Hybridization,|journal=Journal of Heredity|language=en|volume=105|issue=S1|pages=795–809|doi=10.1093/jhered/esu033|issn=0022-1503}}</ref> and examples include e.g. genes involved in olfaction that are introgressed across a ''Mus musculus'' and ''M. domesticus'' hybrid zone.<ref name=":139">{{Citation|last=Teeter|first=K. C.|last2=Payseur|first2=B. A.|last3=Harris|first3=L. W.|last4=Bakewell|first4=M. A.|last5=Thibodeau|first5=L. M.|last6=O'Brien|first6=J. E.|last7=Krenz|first7=J. G.|last8=Sans-Fuentes|first8=M. A.|last9=Nachman|first9=M. W.|date=2007|title=Genome-wide patterns of gene flow across a house mouse hybrid zone|url=http://www.genome.org/cgi/doi/10.1101/gr.6757907|journal=Genome Research|language=en|volume=18|issue=1|pages=67–76|doi=10.1101/gr.6757907|issn=1088-9051|pmc=PMC2134771|pmid=18025268}}</ref> In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f. <ref name=":140">{{Citation|last=Hooper|first=Daniel M.|last2=Griffith|first2=Simon C.|last3=Price|first3=Trevor D.|date=2019|title=Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14874|journal=Molecular Ecology|language=en|volume=28|issue=6|pages=1246–1262|doi=10.1111/mec.14874|issn=0962-1083}}</ref> === Conclusions and future directions === Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization. While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization?<ref name=":44" /><ref name=":72" /> To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. <ref name=":42" /> or are there generally stable solutions with high contributions from both parent species across the genome c.f.? <ref name=":48" /> What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. ?<ref name=":98" /><ref name=":132" /> Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the ''Nicotiana''? <ref name=":99" /> Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation. == Box: Detecting and studying hybridization with genomic tools == Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE,<ref name=":142">{{Citation|last=Pritchard|first=J. K.|last2=Stephens|first2=M.|last3=Donnelly|first3=P.|date=2000|title=Inference of population structure using multilocus genotype data|url=https://www.ncbi.nlm.nih.gov/pubmed/10835412|journal=Genetics|volume=155|issue=2|pages=945–959|issn=0016-6731|pmc=1461096|pmid=10835412}}</ref> ADMIXTURE<ref name=":143">{{Citation|last=Alexander|first=D. H.|last2=Novembre|first2=J.|last3=Lange|first3=K.|date=2009|title=Fast model-based estimation of ancestry in unrelated individuals|url=http://genome.cshlp.org/cgi/doi/10.1101/gr.094052.109|journal=Genome Research|language=en|volume=19|issue=9|pages=1655–1664|doi=10.1101/gr.094052.109|issn=1088-9051|pmc=PMC2752134|pmid=19648217}}</ref> or fineSTRUCTURE.<ref name=":144">{{Citation|last=Lawson|first=Daniel John|last2=Hellenthal|first2=Garrett|last3=Myers|first3=Simon|last4=Falush|first4=Daniel|date=2012|editor-last=Copenhaver|editor-first=Gregory P.|title=Inference of Population Structure using Dense Haplotype Data|url=http://dx.plos.org/10.1371/journal.pgen.1002453|journal=PLoS Genetics|language=en|volume=8|issue=1|pages=e1002453|doi=10.1371/journal.pgen.1002453|issn=1553-7404|pmc=PMC3266881|pmid=22291602}}</ref> These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization.<ref name=":145">{{Citation|last=Lawson|first=Daniel J.|last2=van Dorp|first2=Lucy|last3=Falush|first3=Daniel|date=2018|title=A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots|url=http://www.nature.com/articles/s41467-018-05257-7|journal=Nature Communications|language=en|volume=9|issue=1|doi=10.1038/s41467-018-05257-7|issn=2041-1723|pmc=PMC6092366|pmid=30108219}}</ref> If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests<ref name=":146">{{Citation|last=Kulathinal|first=Rob J.|last2=Stevison|first2=Laurie S.|last3=Noor|first3=Mohamed A. 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W.|last4=Maricic|first4=T.|last5=Stenzel|first5=U.|last6=Kircher|first6=M.|last7=Patterson|first7=N.|last8=Li|first8=H.|last9=Zhai|first9=W.|date=2010|title=A Draft Sequence of the Neandertal Genome|url=http://www.sciencemag.org/cgi/doi/10.1126/science.1188021|journal=Science|language=en|volume=328|issue=5979|pages=710–722|doi=10.1126/science.1188021|issn=0036-8075|pmc=PMC5100745|pmid=20448178}}</ref><ref name=":148">{{Citation|last=Durand|first=Eric Y.|last2=Patterson|first2=Nick|last3=Reich|first3=David|last4=Slatkin|first4=Montgomery|date=2011|title=Testing for Ancient Admixture between Closely Related Populations|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msr048|journal=Molecular Biology and Evolution|language=en|volume=28|issue=8|pages=2239–2252|doi=10.1093/molbev/msr048|issn=1537-1719|pmc=PMC3144383|pmid=21325092}}</ref> or f-statistics.<ref name=":149">{{Citation|last=Peter|first=Benjamin M.|date=2016|title=Admixture, Population Structure, and F -Statistics|url=http://www.genetics.org/lookup/doi/10.1534/genetics.115.183913|journal=Genetics|language=en|volume=202|issue=4|pages=1485–1501|doi=10.1534/genetics.115.183913|issn=0016-6731|pmc=PMC4905545|pmid=26857625}}</ref><ref name=":150">{{Citation|last=Reich|first=David|last2=Thangaraj|first2=Kumarasamy|last3=Patterson|first3=Nick|last4=Price|first4=Alkes L.|last5=Singh|first5=Lalji|date=2009|title=Reconstructing Indian population history|url=http://www.nature.com/articles/nature08365|journal=Nature|language=en|volume=461|issue=7263|pages=489–494|doi=10.1038/nature08365|issn=0028-0836|pmc=PMC2842210|pmid=19779445}}</ref> Modified versions of these tests can be used to infer introgressed genomic regions,<ref name=":151">{{Citation|last=Martin|first=Simon H.|last2=Davey|first2=John W.|last3=Jiggins|first3=Chris D.|date=2015|title=Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu269|journal=Molecular Biology and Evolution|language=en|volume=32|issue=1|pages=244–257|doi=10.1093/molbev/msu269|issn=1537-1719|pmc=PMC4271521|pmid=25246699}}</ref> the direction of gene flow<ref name=":152">{{Citation|last=Pease|first=James B.|last2=Hahn|first2=Matthew W.|date=2015|title=Detection and Polarization of Introgression in a Five-Taxon Phylogeny|url=https://academic.oup.com/sysbio/article/64/4/651/1650669|journal=Systematic Biology|language=en|volume=64|issue=4|pages=651–662|doi=10.1093/sysbio/syv023|issn=1076-836X}}</ref><ref name=":153">{{Citation|last=Eaton|first=Deren A. R.|last2=Ree|first2=Richard H.|date=2013|title=Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)|url=https://academic.oup.com/sysbio/article/62/5/689/1684460|journal=Systematic Biology|language=en|volume=62|issue=5|pages=689–706|doi=10.1093/sysbio/syt032|issn=1076-836X|pmc=PMC3739883|pmid=23652346}}</ref> or the amount of gene flow.<ref name=":150" /> For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited.<ref name=":154">{{Citation|last=Pickrell|first=Joseph K.|last2=Pritchard|first2=Jonathan K.|date=2012|editor-last=Tang|editor-first=Hua|title=Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1002967|journal=PLoS Genetics|language=en|volume=8|issue=11|pages=e1002967|doi=10.1371/journal.pgen.1002967|issn=1553-7404|pmc=PMC3499260|pmid=23166502}}</ref><ref name=":155">{{Citation|last=Patterson|first=Nick|last2=Moorjani|first2=Priya|last3=Luo|first3=Yontao|last4=Mallick|first4=Swapan|last5=Rohland|first5=Nadin|last6=Zhan|first6=Yiping|last7=Genschoreck|first7=Teri|last8=Webster|first8=Teresa|last9=Reich|first9=David|date=2012|title=Ancient Admixture in Human History|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.145037|journal=Genetics|language=en|volume=192|issue=3|pages=1065–1093|doi=10.1534/genetics.112.145037|issn=0016-6731|pmc=PMC3522152|pmid=22960212}}</ref><ref name=":156">{{Citation|last=Lipson|first=Mark|last2=Loh|first2=Po-Ru|last3=Levin|first3=Alex|last4=Reich|first4=David|last5=Patterson|first5=Nick|last6=Berger|first6=Bonnie|date=2013|title=Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow|url=https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/mst099|journal=Molecular Biology and Evolution|language=en|volume=30|issue=8|pages=1788–1802|doi=10.1093/molbev/mst099|issn=1537-1719|pmc=PMC3708505|pmid=23709261}}</ref> These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help.<ref name=":157">{{Citation|last=Yu|first=Yun|last2=Barnett|first2=R. Matthew|last3=Nakhleh|first3=Luay|date=2013|title=Parsimonious Inference of Hybridization in the Presence of Incomplete Lineage Sorting|url=https://academic.oup.com/sysbio/article/62/5/738/1685537|journal=Systematic Biology|language=en|volume=62|issue=5|pages=738–751|doi=10.1093/sysbio/syt037|issn=1076-836X|pmc=PMC3739885|pmid=23736104}}</ref><ref name=":158">{{Citation|last=Wen|first=Dingqiao|last2=Yu|first2=Yun|last3=Nakhleh|first3=Luay|date=2016|editor-last=Edwards|editor-first=Scott|title=Bayesian Inference of Reticulate Phylogenies under the Multispecies Network Coalescent|url=https://dx.plos.org/10.1371/journal.pgen.1006006|journal=PLOS Genetics|language=en|volume=12|issue=5|pages=e1006006|doi=10.1371/journal.pgen.1006006|issn=1553-7404|pmc=PMC4856265|pmid=27144273}}</ref> Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination.<ref name=":155" /><ref name=":159">{{Citation|last=Moorjani|first=Priya|last2=Patterson|first2=Nick|last3=Hirschhorn|first3=Joel N.|last4=Keinan|first4=Alon|last5=Hao|first5=Li|last6=Atzmon|first6=Gil|last7=Burns|first7=Edward|last8=Ostrer|first8=Harry|last9=Price|first9=Alkes L.|date=2011|editor-last=McVean|editor-first=Gil|title=The History of African Gene Flow into Southern Europeans, Levantines, and Jews|url=http://dx.plos.org/10.1371/journal.pgen.1001373|journal=PLoS Genetics|language=en|volume=7|issue=4|pages=e1001373|doi=10.1371/journal.pgen.1001373|issn=1553-7404|pmc=PMC3080861|pmid=21533020}}</ref><ref name=":160">{{Citation|last=Moorjani|first=Priya|last2=Sankararaman|first2=Sriram|last3=Fu|first3=Qiaomei|last4=Przeworski|first4=Molly|last5=Patterson|first5=Nick|last6=Reich|first6=David|date=2016|title=A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years|url=http://www.pnas.org/lookup/doi/10.1073/pnas.1514696113|journal=Proceedings of the National Academy of Sciences|language=en|volume=113|issue=20|pages=5652–5657|doi=10.1073/pnas.1514696113|issn=0027-8424|pmc=PMC4878468|pmid=27140627}}</ref><ref name=":161">{{Citation|last=Loh|first=Po-Ru|last2=Lipson|first2=Mark|last3=Patterson|first3=Nick|last4=Moorjani|first4=Priya|last5=Pickrell|first5=Joseph K.|last6=Reich|first6=David|last7=Berger|first7=Bonnie|date=2013|title=Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium|url=http://www.genetics.org/lookup/doi/10.1534/genetics.112.147330|journal=Genetics|language=en|volume=193|issue=4|pages=1233–1254|doi=10.1534/genetics.112.147330|issn=0016-6731}}</ref><ref name=":162">{{Citation|last=Sankararaman|first=Sriram|last2=Patterson|first2=Nick|last3=Li|first3=Heng|last4=Pääbo|first4=Svante|last5=Reich|first5=David|date=2012|editor-last=Akey|editor-first=Joshua M.|title=The Date of Interbreeding between Neandertals and Modern Humans|url=https://dx.plos.org/10.1371/journal.pgen.1002947|journal=PLoS Genetics|language=en|volume=8|issue=10|pages=e1002947|doi=10.1371/journal.pgen.1002947|issn=1553-7404|pmc=PMC3464203|pmid=23055938}}</ref> With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa.<ref name=":163">{{Citation|last=Pinho|first=Catarina|last2=Hey|first2=Jody|date=2010|title=Divergence with Gene Flow: Models and Data|url=http://www.annualreviews.org/doi/10.1146/annurev-ecolsys-102209-144644|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=41|issue=1|pages=215–230|doi=10.1146/annurev-ecolsys-102209-144644|issn=1543-592X}}</ref> Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum<ref name=":164">{{Citation|last=Excoffier|first=Laurent|last2=Dupanloup|first2=Isabelle|last3=Huerta-Sánchez|first3=Emilia|last4=Sousa|first4=Vitor C.|last5=Foll|first5=Matthieu|date=2013|editor-last=Akey|editor-first=Joshua M.|title=Robust Demographic Inference from Genomic and SNP Data|url=https://dx.plos.org/10.1371/journal.pgen.1003905|journal=PLoS Genetics|language=en|volume=9|issue=10|pages=e1003905|doi=10.1371/journal.pgen.1003905|issn=1553-7404|pmc=PMC3812088|pmid=24204310}}</ref><ref name=":165">{{Citation|last=Gutenkunst|first=Ryan N.|last2=Hernandez|first2=Ryan D.|last3=Williamson|first3=Scott H.|last4=Bustamante|first4=Carlos D.|date=2009|editor-last=McVean|editor-first=Gil|title=Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data|url=https://dx.plos.org/10.1371/journal.pgen.1000695|journal=PLoS Genetics|language=en|volume=5|issue=10|pages=e1000695|doi=10.1371/journal.pgen.1000695|issn=1553-7404|pmc=PMC2760211|pmid=19851460}}</ref> or with summary statistics in an Approximate Bayesian Computation framework.<ref name=":166">{{Citation|last=Beaumont|first=Mark A.|date=2010|title=Approximate Bayesian Computation in Evolution and Ecology|url=https://doi.org/10.1146/annurev-ecolsys-102209-144621|journal=Annual Review of Ecology, Evolution, and Systematics|volume=41|issue=1|pages=379–406|doi=10.1146/annurev-ecolsys-102209-144621}}</ref> It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.<ref name=":167">{{Citation|last=Theunert|first=Christoph|last2=Slatkin|first2=Montgomery|date=2017|title=Distinguishing Recent Admixture from Ancestral Population Structure|url=https://academic.oup.com/gbe/article/2982377/Distinguishing|journal=Genome Biology and Evolution|language=en|volume=9|issue=3|pages=427–437|doi=10.1093/gbe/evx018|issn=1759-6653|pmc=PMC5381645|pmid=28186554}}</ref> ==Glossary== * '''Ancestry block/introgression tracts''' - a region in the genome of a hybrid where all alleles are inherited from the same parent species. * '''[[w:allopolyploid species|Allopolyploid species]]''' - a polyploid hybrid species where the two chromosome sets are derived from different parent species. * '''[[w:backcrossing|Backcrossing]]''' - crossing of a hybrid with one of its parent species. * '''Extrinsic incompatibilities''' - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments. * '''Genome stabilization''' - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased. * '''[[w:Hybrid (biology)|Hybrid]]''' - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species. * '''Hybrid genome''' - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages. * '''[[w:hybrid zone|Hybrid zone]]''' - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring. * '''[[w:Homoploid hybridization|Homoploid hybridization]]''' - the formation of a hybrid with no change in chromosome number. * '''[[w:incomplete lineage sorting|Incomplete lineage sorting]]''' - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles. * '''[[w:introgressive hybridization|Introgressive hybridization]]''' - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing. * '''Intrinsic incompatibilities''' - environment-independent reproductive barriers. * '''[[w:linkage disequilibrium|Linkage disequilibrium]]''' - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci. * '''[[w:Phenology|Phenology]]''' - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions. * '''[[w:Polyploid hybridization|Polyploid hybridization]]''' - the formation of a hybrid involving whole genome duplication. * '''[[w:postzygotic incompatibility|Postzygotic incompatibilities]]''' - reproductive barrier arising after zygote formation, including inviability and sterility. * '''Post-mating barriers''' - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers). * '''Pre-mating barriers''' - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats. * '''[[w:prezygotic incompatibility|Prezygotic incompatibilities]]''' - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization. * '''[[w:reproductive isolation|Reproductive isolation]]''' - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against. * '''[[w:recombination rate|Recombination rate]]''' - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome. * '''[[w:recombinational hybrid speciation|Recombinational hybrid speciation]]''' - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon. * '''[[w:transgressive phenotypes|Transgressive phenotypes]]''' - extreme phenotypes in hybrids, exceeding trait values of both parent lineages. == Wikipedia links == *[[w:Hybrid_(biology)| Hybrid]] *[[w:Polyploidy | Polyploidy]] *[[w:Haldane%27s_rule | Haldane's rule]] *[[w:Genetic_recombination | Recombination]] = References = <references /> cap3pza4krue9dfxhtf9yymqunwdee9