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. 2021 Feb 18;75(4):764–778. doi: 10.1111/evo.14181

Comparative studies on speciation: 30 years since Coyne and Orr

Daniel R Matute 1,, Brandon S Cooper 2
PMCID: PMC8247902  NIHMSID: NIHMS1713885  PMID: 33491225

Abstract

Understanding the processes of population divergence and speciation remains a core question in evolutionary biology. For nearly a hundred years evolutionary geneticists have characterized reproductive isolation (RI) mechanisms and specific barriers to gene flow required for species formation. The seminal work of Coyne and Orr provided the first comprehensive comparative analysis of speciation. By combining phylogenetic hypotheses and species range data with estimates of genetic divergence and multiple mechanisms of RI across Drosophila, Coyne and Orr's influential meta‐analyses answered fundamental questions and motivated new analyses that continue to push the field forward today. Now 30 years later, we revisit the five questions addressed by Coyne and Orr, identifying results that remain well supported and others that seem less robust with new data. We then consider the future of speciation research, with emphasis on areas where novel methods and data motivate potential progress. While the literature remains biased towards Drosophila and other model systems, we are enthusiastic about the future of the field.

Keywords: Speciation, Haldane's rule, Postyzygotic isolation


Speciation is the process in which populations diverge into groups that cease to exchange alleles. A crucial aspect of speciation is the development of reproductive isolating barriers that reduce gene flow between incipient species, although reproductive isolation (RI) is not essential for divergence (Turelli et al. 2001; Nosil 2008). The connection between speciation and the evolution of RI was championed by both Dobzhansky (Dobzhansky 1937) and Mayr (1942), but was earlier developed by Poulton (1904) and Wallace (1865; both reviewed in Mallet 2004). Evolutionary geneticists have characterized reproductive isolating barriers for over 100 years (Dobzhansky 1937; Mayr 1963; Coyne and Orr 2004; Sobel et al. 2010; Nosil 2012), focusing on when barriers occur in the reproductive cycle. Prezygotic barriers occur before a zygote is formed and include ecological barriers (e.g., habitat differences, Sobel et al. 2010), behavioral barriers (e.g., signaling differences, Wilkins et al. 2013; Schaefer and Ruxton 2015), mechanical barriers (e.g., genitalia differences, Grant 1994; Sota and Tanabe 2010), and gametic incompatibilities (Howard 1999). Barriers that occur after fertilization but before a zygote is formed are called postmating‐prezygotic (PMPZ; Howard 1999; Coyne and Orr 2004). Postzygotic barriers occur after a hybrid zygote is formed and include phenotypes as extreme as hybrid sterility and inviability (Orr and Presgraves 2000; Orr 2005; Orr et al. 2007), but also more nuanced traits, such as hybrid behavioral defects (Turissini et al. 2017; McQuillan et al. 2018) or delays in development (Burton 1990; Matute and Coyne 2010). Understanding the evolution of RI is crucial to explain how variation within populations is converted to variation between populations to generate species.

Meta‐analyses have been a productive avenue to study the speciation process. Early studies evaluated the extent of developmentally‐based (intrinsic) postzygotic isolation in groups with different levels of differentiation (Zouros 1973; Ayala et al. 1974; Wilson et al. 1974; Prager and Wilson 1975). While Zouros (1973) found no correlation between genetic distance and the degree of postzygotic isolation, Ayala found that higher taxonomic units showed more isolation than lower units. But it was the seminal comparative analysis of Coyne and Orr (1989) (hereafter, “C&O”) that combined phylogenetic hypotheses with range data, divergence estimates, and empirical estimates of premating and intrinsic postzygotic isolation to rigorously test some of the most important questions in speciation research for the first time. By using published data from 119 Drosophila interspecific hybridizations and their genetic distances, C&O (1989) was the first study to incorporate measurements of hybrid laboratory fitness with molecular divergence.

The importance of C&O (1989) on the field of speciation research is hard to overstate. C&O (1989) gave rise to a cottage industry of similar meta‐analyses, each focused on particular aspects of the speciation process. Researchers have and continue to re‐analyze the data that C&O (1989) assembled to ask specific questions about speciation. These include analysis of how and when Haldane's rule (i.e., the absence, rarity, or sterility of the heterogametic sex in interspecific crosses) appears (Turelli and Begun 1997), correlations between pre‐ and postmating isolation with allozyme and silent DNA divergence (Fitzpatrick 2002), and the influence of ecological divergence on prezygotic and intrinsic postzygotic RI evolution (Funk et al. 2006). These data have also been used to test for reinforcing natural selection on prezygotic isolation in areas of sympatry as a response to maladaptive hybridization (Dobzhansky 1937; Dobzhansky 1940; Blair 1955). Analyses of reinforcement have focused on the role of range overlap (Nosil 2013) and “concordant isolation asymmetries” (Yukilevich 2012), in addition to the relative roles of intrinsic postzygotic isolation, ecological differentiation, and X chromosome size in speciation (Turelli et al. 2014). C&O themselves revisited these data, adding an additional 52 interspecific Drosophila hybridizations to their original dataset (Coyne and Orr 1997). Now 30 years later, we revisit the impact of C&O (1989) on the field.

The Five Original Questions

C&O (1989) addressed five core questions about the speciation process in Drosophila: (i) how rapidly does RI evolve, (ii) do prezygotic and postzygotic isolation evolve at the same rate, iii) do hybrid sterility and inviability evolve at the same rate, iv) how does postzygotic isolation increase with time, and v) is prezygotic isolation enhanced by natural selection when populations become sympatric? In the last 30 years since the publication of C&O (1989), these five questions have become an integral part of the field of speciation biology. We revisit each question, describing the progress made and the importance of the results to the field. We also propose future directions, including limitations that are likely to limit progress in some areas. Even though C&O (1989)’s original piece was published just over 30 years ago, the approaches, the datasets, and the concepts they proposed still spark controversy and remain as relevant today as they were at the time of publication.

HOW RAPIDLY DOES RI EVOLVE?

C&O stated that “the divergence time of taxa must obviously be correlated with the amount of reproductive isolation between them, because all species begin as populations that are not reproductively isolated”. In spite of some earlier precedents (Zouros 1973; Ayala et al. 1974), C&O (1989) was the first study to demonstrate this correlation using data on the magnitude of RI and pairwise genetic distance compiled by them and others (Bock 1984). Importantly, C&O (1989) incorporated phylogenetic corrections to the study of RI, which is crucial given that amounts of isolation among species pairs may not be evolutionarily independent due to their relatedness (Huey and Pianka 1981; Felsenstein 1985). C&O (1989) relied on published phylogenies (Throckmorton 1975, 1982; MacIntyre and Collier 1986) and a procedure inspired by Felsenstein (1985) to correct their data (reviewed in Huey et al. 2019), allowing only one comparison between the species on either side of a phylogenetic bifurcation (Fig. 3 in C&O). This phylogenetic correction ultimately reduced the data from 119 interspecific hybridizations to 42.

C&O (1989) found a monotonic increase in both prezygotic and postzygotic RI as divergence increases between species (Figs. 2 and 4 in C&O), a pattern that has been repeatedly tested and supported across divergent taxa (reviewed in Edmands 2002; Gourbière and Mallet 2010; Coughlan and Matute 2020). In addition to Drosophila (Coyne 1989; Coyne and Orr 1997; Turissini et al. 2018), the pattern of rapid behavioral evolution seems to apply to Etheostoma fish (Mendelson 2003) and Desmognathus salamanders (Tilley et al. 1990). Few examples have addressed the rate of evolution of the particular traits involved in prezygotic isolation. In Mormyd fish, differentiation in sexual cues (electric signals) increases with phylogenetic divergence and usually outpaces differentiation in ecologically important traits (Arnegard et al. 2010). Similarly, in Australian field cricket species (Teleogryllus spp.), male song becomes more differentiated as divergence accrues (Moran et al. 2020). In Etheostoma fish male conspecific preference appears at lower genetic distances than female conspecific preference (Mendelson et al. 2018). This pattern of increasing trait differentiation with genetic distance is not universal. The magnitude of interspecific differences in courtship song in Drosophila (Gleason and Ritchie 1998), and bird plumage coloration (Campagna et al. 2012; Moran et al. 2017) does not increase as divergence accrues. In cichlids, for example, assortative mating is more correlated with ecological niche and morphology than with genetic distance (Stelkens and Seehausen 2009). Since premating isolation is often the result of multimodal signaling (e.g., Ritchie and Gleason 1995; Nosil and Hohenlohe 2012), it is likely that no individual trait will show an increase over time, but the combination of traits might.

More support exists for increasing postzygotic RI with genetic distance, possibly because more taxa have been sampled. Multiple reviews have compiled cases of postzygotic isolation across divergence (Edmands 2002; Gourbière and Mallet 2010; Coughlan and Matute 2020), finding that a monotonic increase in the strength of hybrid inviability and sterility is common. However, there are also exceptions to the rule; for example, hybrid inviability in darters shows no systematic increase with genetic distance, caused in part by the occurrence of hybrid vigor at intermediate levels of divergence (Mendelson 2003). In stalk‐eyed flies hybrid male and female sterility increase with genetic distance but male hybrid inviability does not (Charistianson et al. 2005). Prezygotic isolation in orchids showed no increase over genetic distance for different reasons. While premating isolation in food‐deceptive orchids and PMPZ in food‐ and sexually‐deceptive orchids show variation but no correlation with divergence, sexually deceptive orchids display universally strong premating isolation since very early stages of divergence (Scopece et al. 2007; but see Sobel and Randle 2009 and Scopece et al. 2009). While increasing RI with genetic distance is not universal, the majority of cases suggest a positive correlation between the strength of RI and the genetic distance between species pairs.

While a primary focus since as early as the 19th century (Darwin 1859, Ch. 8 pp. 245–278), hybrid sterility and inviability are not the only forms of postzygotic RI. A broad range of traits can result in reduced hybrid fitness, including aberrant hybrid migratory behavior (Delmore and Irwin 2014), transgressive mating behavior (Gottsberger and Mayer 2007; Clark et al. 2010; Kost et al. 2016), decreased attractiveness (Naisbit et al. 2001; Lemmon and Lemmon 2010; Serrato‐Capuchina et al. 2020), and lower ability to locate a suitable substrate (Linn et al. 2004; Bendall et al. 2017; Turissini et al. 2017). Some evidence suggests that the likelihood that hybrids show transgressive phenotypic values in traits associated with species recognition increases as parental divergence between parentals increases (Stelkens et al. 2009). Phenotypic mismatch in hybrids may also generate postzygotic isolation (McBride and Singer 2010; Singer and McBride 2010; Arnegard et al. 2014; Cooper et al. 2018). For example, hybrids produced by D. yakuba and the forest species D. teissieri on the island of Bioko in West Africa prefer warm and dry habitats like D. yakuba, but they have low desiccation tolerance like D. teissieri, leaving them physiologically ill equipped to perform in their chosen habitat (Cooper et al. 2018). While these studies demonstrate that other postzygotic defects may exist in hybrids, the rates at which they evolve remain understudied.

Ecologically based postzygotic isolation and behavioral defects both increase with divergence, but these studies are substantially rarer than those involving hybrid inviability and hybrid sterility. Habitat isolation in either its premating (e.g., habitat divergence) or postzygotic (e.g., hybrid inviability; Funk et al. 2006) forms, ability to colonize hosts (Vienne et al. 2009), and subtle forms of postzygotic isolation (Turissini et al. 2017) also accrue with genetic distance. To date, most studied barriers to gene flow increase with divergence, albeit their rates of accumulation differ.

DO PRE‐ AND POSTZYGOTIC ISOLATION EVOLVE AT THE SAME RATE?

C&O (1989) also compared the rates of evolution of premating and postzygotic isolation in order to “know which type of isolation is most important in reducing gene flow between incipient species” (page 363). Their analysis demonstrated that premating RI accumulates faster than postzygotic RI, especially in recently diverged species (Fig. 5 in C&O). Unlike the first prediction, that RI should increase with genetic divergence, few explicit tests have compared the rates of evolution of different types of barriers to gene flow. Besides C&O (1989) we found only eight studies (nine clades) that have compared the rate of evolution of different RI barriers (Table 1); premating RI evolved faster than postzygotic RI in five of the examined taxa (Etheostoma darters, Drosophila, Gasterosteus sticklebacks, food‐deceptive orchids, and sexually deceptive‐orchids; Table 1). The analysis of Strepanthus jewelflowers is notable because it is the first attempt to compare the rate of accumulation of ecological divergence (scored as climatic variables) with premating (phenology and floral distance), PMPZ (fruit set), and postzygotic traits (seed‐set success, seed mass, and F1 survival to flowering; Christie and Strauss 2018), demonstrating that niche differences tend to be stronger than other barriers in early stages of divergence. In Cyrtodiopsis stalk‐eyed flies, hybrid sterility evolves faster than premating and other types of RI (Charistianson et al. 2005), and in Nolana bellflowers postzygotic RI is stronger and evolves faster than prezygotic isolation (Jewell et al. 2012). In three more instances (Silene and Glycine, Moyle et al. 2004; and food‐deceptive orchids, Scopece et al. 2007, Scopece et al. 2008) prezygotic and postzygotic RI accumulate at similar rates. Thus, and although the plurality of studied taxa shows faster prezygotic than postzygotic RI, this pattern is not universal.

Table 1.

Studies that have compared the rate of evolution of different RI barriers

Taxon Number of species pairs Result Phylogenetic correction Reference
Darters Etheostoma 13 Sexual isolation accumulates faster than postzygotic RI. Hybrid inviability does not increase over time. Species pair selected to be strictly phylogenetically independent (Mendelson 2003)
Stickleback Gasterosteus 5 Sexual and ecological isolation accumulate faster than other barriers No (Lackey and Boughman 2017)
Streptanthus 39 Climatic niche differences are substantial early in speciation and evolve faster than differences in phenology and floral morphology. Node‐weighted average phylogenetic correction, (Fitzpatrick 2002) (Christie and Strauss 2018)
Nolana 15‐22 Prezygotic pollen–pistile isolation accumulates slower than all postzygotic barriers. Node‐weighted average phylogenetic correction, (Fitzpatrick 2002) (Jewell et al. 2012)
Drosophila 72 Prezygotic and postmating‐prezygotic RI accumulate faster than postzygotic barriers. Random sampling of strictly phylogenetically independent species pairs and bootstrapping (Turissini et al. 2018)
Glycine 18‐55 Postmating‐prezygotic and postzygotic RI accumulate at similar rates. Random sampling of strictly phylogenetically independent species pairs and bootstrapping (Moyle et al. 2004)
Silene 19‐49 Postmating‐prezygotic and postzygotic RI accumulate at similar rates. Random sampling of strictly phylogenetically independent species pairs and bootstrapping (Moyle et al. 2004)
Food‐deceptive orchids 110, 125 Premating and postmating‐prezygotic RI show no clear increase over divergence. Postzygotic RI evolves in a clock‐like manner. Node‐weighted average phylogenetic correction, (Fitzpatrick 2002) and identification of strictly phylogenetically independent species pairs (Scopece et al. 2007)
Sexually deceptive orchids 36 Strong premating RI but weak postmating RI Node‐weighted average phylogenetic correction, (Fitzpatrick 2002) and identification of strictly phylogenetically independent species pairs (Scopece et al. 2007)
Stalk‐eyed flies 12 Hybrid male sterility accumulates faster than premating RI, hybrid inviability, and female hybrid sterility No (Charistianson et al. 2005)

Even though most studies have focused on comparing rates of evolution of prezygotic and postzygotic RI, other traits likely influence how species form and persist. Moyle et al. (2004) presented the first comparative study of RI in plants, and by doing so carried out the first analyses of PMPZ traits (post‐pollination prezygotic traits in the case of plants). For both Glycene and Silene, PMPZ and postzygotic traits evolve at similar rates (Moyle et al. 2004). Four studies have addressed the rate of accumulation of PMPZ barriers. The evolution of PMPZ and postzygotic RI in orchids varies across groups (Scopece et al. 2008). Postzygotic RI increases with divergence in food‐deceptive orchids, but not in sexually‐deceptive ones, but PMPZ does not increase with genetic distance for either type. In Streptanthus and Nolana, fruit set, a metric of whether pollen is able to germinate down the style and fertilize ovules, is not correlated with genetic distance (Jewell et al. 2012; Christie and Strauss 2018). Finally, in Drosophila, PMPZ RI evolves almost as fast as premating RI (Turissini et al. 2018). Differences among the rates of evolution of PMPZ RI in these few divergent taxa highlight the need for additional sampling to better understand the contribution of PMPZ barriers to species persistence as divergence increases.

More generally, premating barriers accumulate fast in multiple taxa. Yet, in other taxa, postzygotic RI accumulates as fast or faster than prezygotic RI. In the case of hybrid zones, some have argued that premating isolation is the most effective mechanism in keeping species apart (e.g., Kirkpatrick and Ravigné, Jiggins et al. 2001), while others argue that premating isolation alone is ineffective at maintaining species boundaries (Irwin 2020). In all likelihood, premating, PMPZ, and postzygotic RI act in conjunction to maintain species boundaries in nature (Servedio and Saetre 2003; Widmer et al. 2009; Schemske 2010), and the relative importance and order of appearance of different barriers will vary across taxa.

DO HYBRID STERILITY AND INVIABILITY EVOLVE AT THE SAME RATE?

C&O (1989) next asked whether hybrid sterility and inviability evolve at different rates. This seems plausible given that hybrid sterility and inviability need not share genetic and/or developmental bases (Orr 1993, Sawamura 2000, Bundus et al. 2018; but see Barbash and Ashburner 2003, Sawamura et al. 2014), and that mechanisms of postzygotic RI may have a complex genetic basis (Matute et al. 2014; Phadnis et al. 2015; Barnard‐Kubow and Galloway 2017; Larson et al. 2018). Using a similar approach that they used to compare rates of evolution of prezygotic and postzygotic RI, C&O (1989) found that hybrid sterility and inviability evolve at similar rates, suggesting that these barriers are “by‐products of similar genetic processes” and equally likely to underlie the persistence of incipient Drosophila species. However, more recent work found that sterility accumulates faster than inviability (Wu 1992; Coyne and Orr 1997; Turissini et al. 2018). This discrepancy seems to result from how the data are analyzed, with average time of divergence between species pairs being an underpowered measure to assess differences in rates of evolution of different types of RI (Wu 1992; Coyne and Orr 1997; Coyne and Orr 2004, p. 75).

Five additional cases in non‐Drosophila taxa provide support for faster evolution of sterility than inviability. Using data collected on mammals (Gray 1972), Wu (1992) found 25 instances of Haldane's rule for sterility, but no good cases of Haldane's rule for inviability. Similarly, the mean age of Lepidopteran (Presgraves 2002), bird (Price and Bouvier 2002), and frog (Sasa et al. 1998) species showing hybrid sterility is lower than the mean age of species showing hybrid inviability. The rate of evolution of complete hybrid sterility is higher than the rate of accumulation of embryo mortality in food‐deceptive Mediterranean orchids (Scopece et al. 2008); and in Cyrtodiopsis stalk‐eyed flies, male hybrid sterility accumulates faster than hybrid inviability, hybrid female sterility, and premating RI (Charistianson et al. 2005). This rapid evolution of hybrid sterility in stalk‐eyed flies has been interpreted as evidence of pervasive genetic conflict (Charistianson et al. 2005). Introgression analyses in Drosophila have suggested that regions that cause hybrid sterility are much more abundant than regions that cause hybrid inviability (True et al. 1996; Masly and Presgraves 2007). Even though to date all studied taxa show evidence of faster evolution of hybrid sterility than inviability, given the small number of comparative studies addressing the relative rates of accumulation of different postzygotic barriers, the question of whether sterility evolves faster than inviability seems far from settled. Even if inviability evolves relatively slowly, it is worth noting that changes to the regulation of morphological development can evolve rapidly (Abzhanov et al. 2004; Shapiro et al. 2004; Mallarino and Abzhanov 2012), and hybrid inviability appears earlier in some taxa (e.g., mammals) than others (e.g., birds) (Prager and Wilson 1975; Fitzpatrick 2004), due in part to parent‐of‐origin‐dependent abnormal growth (Vrana et al. 2000; Ishikawa et al. 2011; Brekke and Good 2014; Rebernig et al. 2015; Oneal et al. 2016; Coughlan et al. 2020).

Both sterility and inviability are developmental defects that can manifest at different stages of development (Cutter and Bundus 2020). Analyses of gene expression across development suggest an “hourglass” model with increased divergence at intermediate developmental stages (Cruickshank and Wade 2008; Kalinka et al. 2010; Liu et al. 2019). To our knowledge, no analysis of gene expression across hybrid development exists, but the hourglass model predicts incompatibility to arise at early and late stages. Only two studies have dissected components of hybrid inviability across development. Closely related Bufo toad species produce hybrids that are more likely to reach later developmental stages than hybrids produced by more diverged pairs, which suggests that hybrid inviability at later stages of development evolves slower (Malone and Fontenot 2008). In Drosophila, embryonic inviability evolves before larval or pupal inviability (Turissini et al. 2018), and mapping of X‐linked incompatibilities reveals a higher number of embryonic and pupal incompatibilities than larval incompatibilities in hybrids between diverged species (Matute and Gavin‐Smyth 2014).

It is worth noting one important caveat about the comparison of the rate of accumulation of inviability and sterility (or between different developmental stages). Because sterility can only occur in viable hybrids, the range of genetic distances in which we can observe sterility is necessarily smaller than the range for inviability (Wu 1992; Coyne and Orr 2004 pp. 57–60). Similar issues also apply to the study of other traits; for example, in cases where behavioral isolation is complete, collecting information on the strength of postzygotic RI is unfeasible (but see Sánchez and Santamaria 1997). In summary, and in contrast to the original C&O (1989) result, current evidence suggests that hybrid sterility accumulates faster than inviability, but more work in additional taxa are needed to settle this question.

HOW DOES POSTZYGOTIC ISOLATION INCREASE WITH TIME?

C&O (1989) built on their analysis of rates of hybrid sterility and inviability evolution by asking if these barriers increase with divergence time, and if so, whether they accumulate at different rates between the sexes. Analyses of postzygotic RI have generally found that in dioecious species, the sterile or inviable sex tends to be the heterogametic sex, a pattern known as “Haldane's rule” (Haldane 1922). Multiple genetic mechanisms for Haldane's rule have been proposed (reviewed in Wu et al. 1996; Laurie 1997; Orr 1997; Schilthuizen et al. 2011; Delph and Demuth 2016) and supported (Orr 1993; Masly and Presgraves 2007). There are relatively few exceptions, making Haldane's rule one of the only speciation “rules”. Indeed, of 223 cases of hybrid sterility in dioecious animals, 213 follow Haldane's rule. Of 452 cases of hybrid inviability, also in dioecious animals, 381 follow Haldane's rule (Table 2 in Schilthuizen et al. 2011). The rule applies to animal species with heteromorphic and homomorphic sex chromosomes (Presgraves and Orr 1998). C&O (1989) tested whether Haldane's rule appears early in the speciation process by evaluating genetic divergence between species that produce sterile or inviable hybrid males, sterile or inviable females, or sterility and inviability in both sexes. One would expect that if Haldane's rule is common it must necessarily precede the case where both sexes are sterile or inviable. Of the 21 pairs of recently diverged species, they evaluated after phylogenetic corrections, 19 produced hybrids whose sterility and inviability is limited to the heterogametic sex. The results suggest that male sterility and inviability evolve prior to hybrid female defects (Coyne 1989; Coyne and Orr 1997; but see Turissini et al. 2018).

A follow‐up approach in Drosophila found that in the melanogaster species complex, defects pertaining to males accumulate faster than those of females. Hybrid male inviability evolves faster than hybrid female inviability, and hybrid male sterility evolves faster than hybrid female sterility (Turissini et al. 2018). Contrary to the C&O (1989) findings, female sterility seems to evolve at lower genetic distances than male inviability (Turissini et al. 2018). Systematic introgressions between Drosophila species have revealed a higher number of hybrid male sterility alleles than of hybrid female sterility alleles (True et al. 1996; Sawamura et al. 2000; Masly and Presgraves 2007). Outside Drosophila, few studies have addressed which hybrid defects accumulate faster in the heterogametic sex. In birds, male F1 sterility appears earlier than female inviability. Cases of Haldane's rule for sterility are five times more common than for inviability (Price and Bouvier 2002; Arrieta et al. 2013). In Lepidopterans, hybrid female inviability often evolves prior to hybrid male sterility (Presgraves 2002). Additional analyses of when and how Haldane's rule appears during speciation are needed.

In species with chromosomal sex determination, comparative studies of the effects of sex chromosomes on interspecific hybrid fitness suggest that large sex chromosomes accumulate more hybrid incompatibilities than do smaller sex chromosomes. X‐linked incompatibilities often underlie intrinsic postzygotic isolation and Haldane's rule in Drosophila (Orr 1993; Good et al. 2008; Presgraves 2008, 2018; Meiklejohn and Tao 2010; Muirhead and Presgraves 2016), and Drosophila species pairs with relatively larger X chromosomes evolve Haldane's rule faster (Turelli and Begun 1997). Lepidopterans show a categorically different pattern. Despite having small sex chromosomes (comparable with Drosophila species with small X‐chromosomes; Traut et al. 2007; Kaiser and Bachtrog 2010), Haldane's rule for sterility appears relatively early in Lepidopterans (Presgraves 2002). No similar study has addressed whether heterosomes (i.e., sex chromosomes only present in the heterogametic sex) also correlate with RI. The collective observations of the accumulation of hybrid defects along divergence suggest that Haldane's rule is a common phase in the speciation process.

More generally, the presence of sex chromosomes has been hypothesized to contribute to faster evolution of postzygotic RI (Johnson 2010; Johnson and Lachance 2012; Phillips and Edmans 2012). The evidence for this hypothesis is limited and comes from three sources. First, haplodiploid species, which do not have differentiated sex chromosomes but show Haldane's rule, seem to evolve hybrid incompatibility more slowly than other insects (Koevoets and Beukeboom 2009). Second, using diversification rates and species richness from Eo and DeWoody (2010), Phillips and Edmands (2012) concluded that lizards and snakes (squamates) which have differentiated sex chromosomes have speciated more quickly than turtles and crocodilians, two clades in which differentiated sex chromosomes are rare and absent, respectively. This pattern is not followed by birds that universally possess ZW sex. Finally, a meta‐analysis of 26 species pairs suggests that taxa without sex chromosomes show the slowest rates of evolution of postzygotic RI, but the effect of the presence of sex chromosomes is small (Lima 2014). Sex chromosome turnover is also associated with the evolution of intrinsic postzygotic RI in stickleback fish (Kitano et al. 2009; Kitano and Peichel 2012) and bark beetles (Bracewell et al. 2017). Whether sex chromosomes (including the evolution of neo‐sex chromosomes) and dioecy accelerate the accumulation of RI and speciation rates remains unknown.

IS PREZYGOTIC RI ENHANCED BY SELECTION WHEN POPULATIONS BECOME SYMPATRIC?

Finally, C&O (1989) examined if RI accumulates faster in sympatry versus allopatry. Under this hypothesis known as reinforcement, natural selection may accelerate the speciation process by penalizing maladaptive hybridization, favoring stronger prezygotic RI to avoid maladaptive hybridization in species with overlapping geographical ranges (Liou and Price 1994; Servedio and Noor 2003; Schlichting and Mousseau 2009; Hopkins 2013). Potential costs of hybridization include hybrid defects and costs to females after heterospecific matings (Servedio 2001, 2011; Lorch and Servedio 2005). Importantly, for Drosophila and other species with internal fertilization and external development, only prezygotic RI should be reinforced because selection does not act to increase postzygotic RI in sympatry (Wallace 1889, Ch. 7; Coyne 1974). Multiple cases reported the possibility of reinforcement before C&O (1989) (e.g., Littlejohn 1965; Fouquette Jr 1975; Loftus‐Hills 1975; Markow 1981; Levin 1985). For example, Ehrman (Ehrman 1965) found the first strong support for reinforcement, demonstrating greater premating isolation for most comparisons of sympatric populations of “semispecies” in the D. paulistorum clade (Dobzhansky and Spassky 1959). However, the first large‐scale comparative study to lend evidence to the possibility of pervasive reinforcement across a large taxonomic group was C&O (1989).

To test for reinforcement, C&O (1989) regressed the magnitude of RI on the genetic distance between sympatric and allopatric Drosophila species pairs, independently. In the case of both prezygotic and postzygotic RI, the intercept should be similar as recently diverged species have low costs to hybridization. In contrast, if reinforcement has taken place, RI should accumulate more quickly for sympatric than for allopatric pairs, generating differences in the regression slopes. This is precisely what C&O (1989) found—the mean degree of premating RI, but not postzygotic RI, is twice as large for sympatric species than for allopatric species. This was the first evidence widely supporting reinforcement over competing hypotheses (e.g., differential fusion and extinction; Templeton 1981; Butlin 1987), and served to fuel a body of research on the role of reinforcement in speciation in other systems (Noor 1995; Niet et al. 2006; Hopkins and Rausher 2012; Castillo and Moyle 2019).

In the last 30 years, similar tests have assessed whether reinforcement is pervasive in other clades, and the evidence is mixed. In fungi, homobasidiomycota show a faster accumulation of total RI in sympatric species pairs than in allopatric pairs (Giraud and Gourbière 2012). Evidence for reinforcement also exists in plants (Niet et al. 2006; Grossenbacher and Whittall 2011), although as noted by Hopkins (2013) uncertainty about the role of reinforcement in plant speciation remains due to both approximate and incomplete measures of RI. Comparing RI in sympatric and allopatric species has shown no evidence of reinforcement in Glycine and Silene plants (in either postmating prezygotic or postzygotic, Moyle et al. 2004), ascomycetous fungi (in total isolation, Giraud and Gourbière 2012), or doves (Lijtmaer et al. 2003). Clearly, even if reinforcement is a common step in the completion of speciation, it does not leave a universal signature in sympatric species.

The use of the comparative approach also propelled new tests, all of which are framed within the use of phylogenetically corrected RI datasets. A second test involves identifying triads of species for which the magnitude of RI is known. If one of the species pairs is sympatric and the other allopatric, and reinforcement has acted on the sympatric pair, then the magnitude of RI should be stronger in the sympatric pair (Noor 1997). In spite of the power of this approach triads of species have only been used to infer reinforcement of behavioral isolation in Drosophila (Turissini et al. 2015), bird plumage (Martin et al. 2015), bird body size (Bothwell et al. 2015), and bird chromosomal rearrangements (Hooper and Price 2017). This latter trait might be associated with the likelihood that species in sympatry persist when they have the chance to hybridize, and not associated with reinforcement itself (e.g., Hooper et al. 2019).

A third test using comparative data to infer reinforcement involves identifying species pairs with asymmetric levels of premating and postzygotic RI (Yukilevich 2012). In cases with strong postzygotic RI, the influence of reinforcing selection should be strong due to a high risk of maladaptive hybridization. Throughout nature, the fitness of hybrids produced by reciprocal crosses often differs (Darwin 1859, Ch. 8), generating a pattern of asymmetrical postzygotic RI known as “Darwin's corollary to Haldane's rule” (Turelli and Moyle 2007). In these cases, reinforcing selection should generate elevated prezygotic RI for the side of the cross with stronger postzygotic RI. Yukilevich (Yukilevich 2012) tested this hypothesis and found a pattern of concordant asymmetries is more common in sympatry than in allopatry. This pattern could be caused by reinforcement, or by other processes that favor the co‐occurrence of premating and postzygotic RI simultaneously. For example, asymmetries in gene flow could encourage the asymmetric accumulation of intrinsic postzygotic RI (Turelli et al. 2014). An extension of this approach uses the proportion of overlapping geographic range as a proxy for the risk of hybridization (Nosil 2013). Species pairs that share a larger proportion of their geographic range are more likely to hybridize and thus the proportion of geographic range that two hybridizing species share should be proportional to their RI. Indeed, there is a negative correlation between the strength of premating isolation and geographic overlap which has been interpreted as additional evidence for the role of reinforcement on speciation.

The relative frequency of reinforcement remains a contentious question in speciation (Hudson and Price 2014; Turelli et al. 2014). Reinforcement debates prior to C&O (1989) were mostly centered around whether reinforcing selection is plausible (Paterson 1978; Spencer et al. 1986). Since C&O (1989), the question has been repeatedly re‐evaluated to assess the relative importance of this process in nature. Some have argued that reinforcement is pervasive (Hudson and Price 2014); and given the ubiquity of sympatry in Drosophila (Nosil 2013; Turelli et al. 2014), and the possibility of recapitulating reinforced RI in the laboratory with experimental evolution (Koopman 1950; Rice and Hostert 1993; Etges 1998; Higgie et al. 2000; Matute 2010a,b), Turelli et al. (2014) concluded that reinforcement must be common, at least in Drosophila. While we have no definitive answers yet on how frequently reinforcement acts in speciation, C&O (1989) opened the door to study it in a systematic and comparative manner.

Future Questions

By definition, speciation is at the interface of microevolutionary and macroevolutionary processes. C&O (1989) posed and addressed five questions using the comparative approach. These research avenues are still priorities and represent a large portion of the current speciation research. Still, the field has changed considerably since 1989, and two specific developments seem worth mentioning. First, the infusion of genomic data has revitalized speciation research, giving rise to new hypotheses and methods to test them (Butlin 2010; Rice et al. 2011; Seehausen et al. 2014; Campbell et al. 2018). Second, the field has incorporated robust population genetics and phylogenetic methods to understand diversification over time (reviewed in O'Meara 2012; Pennell and Harmon 2013). The combination of these data and methodological advancements has generated new questions and challenges that can be addressed with variations of the comparative approach. Here, we list five directions that the field is poised to address using a combination of comparative phylogenetic methods, genomics, and natural history.

THE AMOUNT OF INTROGRESSION AS DIVERGENCE PROCEEDS

The converse aspect of the scaling of RI with divergence is that the amount of gene exchange between sympatric taxa should decrease as genetic divergence accrues for two reasons. First, hybrid production decreases as divergence accrues, which reduces the possibility for hybrids to serve as a bridge for gene exchange between parental species. This is supported by the reduction in the number of naturally occurring hybrids as divergence increases (e.g., Mallet 2007; Pereira et al. 2011; Sánchez‐Guillén et al. 2014). Second, hybrids produced by more divergent parents will have more hybrid incompatibilities, thus purging introgression even if hybridization occurs (Orr 1995; Matute et al. 2010; Moyle and Nakazato 2010; Wang et al. 2015). Notably, the decrease in gene exchange might be precipitous across the ‘gray zone of speciation’—the level of differentiation in which species definition is controversial (Roux et al. 2016). Few tests for a relationship between amounts of introgression and the divergence between species pairs exist, but the magnitude of segregating introgression in Phletodon salamander (Wiens et al. 2006), Heliconius butterfly (Kronforst et al. 2013), and Solanum tomato (Hamlin et al. 2020) species pairs is inversely correlated with the age of divergence of the hybridizing species. Whether this is a pattern that applies to other taxa remains unknown.

THE EFFECT OF GENETIC DISTANCE ON HYBRID SPECIATION

Hybrid speciation remains a relatively rare and highly controversial form of speciation (Schumer et al. 2014; Schumer et al. 2018; Nieto Feliner et al. 2017). In this process, hybrid populations become reproductively isolated from the parental forms as a result of admixture (Gross and Rieseberg 2005; Mallet 2007). Since the possibility of hybrid speciation is contingent on the fitness of hybrids from early generations, genetic distance is a factor that might determine the likelihood of the process. Hybridization could fuel adaptive radiations, but how the genetic distance between hybridizing species influences the likelihood of hybrid speciation remains largely understudied (Seehausen 2004; Meier et al. 2017; Marques et al. 2019). Multiple theoretical models have proposed mechanisms on how hybrid speciation might proceed (Buerkle et al. 2000; Schumer et al. 2015; Blanckaert and Bank 2018; Comeault 2018; Yamaguchi and Otto 2020), but few empirical studies exist. In plants, the likelihood of allopolyploidy depends on the magnitude of genetic divergence (Chapman and Burke 2007; Paun et al. 2009); and in experimentally produced, admixed populations of Drosophila that differed in their degree of genetic relatedness (Comeault and Matute 2018), hybrid swarms from parents with intermediate levels of divergence were most likely to become reproductively isolated from the parental species. These two results suggest that intermediate levels of divergence might be more permissive for speciation by hybridization and that, as proposed by the theoretical models, there might be a level of genome divergence that facilitates hybrid speciation. As is the case with the relative prevalence of hybrid speciation in evolution, the importance of genomic traits such as recombination rates, presence of sex chromosomes, and chromosomal rearrangements for the formation of hybrids species remains largely unknown.

COMPARATIVE RATES OF EVOLUTION ACROSS DIFFERENT TAXA

RI could limit rates of diversification across taxa (Mayr 1963). If so, taxa should vary in their rate of RI acquisition, and groups with a greater propensity to evolve RI should become more speciose. This question precedes C&O (1989) and remains unsolved today. Seminal work revealed that hybrid inviability evolves faster in mammals than in birds and frogs, which was attributed to rapid regulatory evolution in mammals (Wilson et al. 1974; Prager and Wilson 1975; Fitzpatrick 2004). More recent taxon‐specific comparisons have demonstrated that postzygotic RI evolves faster in Drosophila and in Lepidoptera than in anurans (Russell 2003; Mendelson et al. 2004). Few studies have formally tested whether taxa displaying faster RI evolution also harbor more species. Meta‐analyses have failed to find a relationship between the strength of assortative mating and species richness (Janicke et al. 2019). New comparative phylogenetic methods have revitalized this question. Nodal‐network models suggest that RI from pairwise crosses can be used to estimate the strength of RI as an individual species trait (i.e., whether a single species is more prone to being isolated from all other species). Drosophila and bird species differ significantly in their RI as a species trait—some species evolve RI more quickly than others (Rabosky and Matute 2013). Similar results, in terms of the per branch speciation rate, have been reported in lizards (Singhal et al. 2018). Notably, there is no correlation between the rates of RI acquisition and diversification rates in Drosophila or birds. Together, these results suggest that the rate of RI evolution might not be the factor limiting the evolution of new species. In turn, the persistence of species when they have the chance to hybridize (and go extinct) might play an important role in determining species richness (Rosenblum et al. 2012; Harvey et al. 2019). This direction will benefit from a systematic study of RI across taxa, the generation of robust time‐calibrated phylogenies, and the collection of generation times, which will jointly enable modeling RI under various models of trait evolution (Moyle and Payseur 2009; Huey et al. 2019).

MACROEVOLUTIONARY METRICS OF DIVERSIFICATION

RI might also be associated with global patterns of biodiversity (Mayr 1963; Rabosky 2016). There are more species in the tropics than in temperate areas, which generates questions about the relative contributions of speciation and extinction rates to this pattern, including how they vary spatially (reviewed in Willig et al. 2003; Schemske et al. 2009; Jablonski et al. 2017). The rates of evolution of traits that differentiate species vary clinally with latitude. In birds, climatic‐niche (Lawson and Weir 2014) and bird song traits (Weir and Wheatcroft 2011) evolve faster at higher latitudes, yet studies comparing rates of RI acquisition in tropical and temperate species are rare. Only one study has tested whether RI evolves faster between tropical than between temperate species. Yukilevich (Yukilevich 2013) found that, after controlling for genetic distance, species pairs in the tropics display stronger hybrid sterility than species in temperate areas. (This pattern does not exist for premating RI.) The connection between metrics of diversification and RI remains in its infancy, but it is one of the most urgent questions in speciation biology. Similar to the need for robust time‐calibrated phylogenies to understand whether clades differ in how RI accumulates, only a systematic study of the accumulation of RI across taxa and of species richness across time will reveal whether the acquisition of RI influences the rate of speciation at macroevolutionary scales.

DARWIN'S COROLLARY TO HALDANE'S RULE

Reciprocal crosses often differ in the magnitude of RI as described above (Tiffin et al. 2001; Turelli and Moyle 2007; Lowry et al. 2008). While C&O (1989) did not address this pattern, theoretical models (Turelli and Moyle 2007) and a handful of empirical examples (Sawamura and Yamamoto 1993; Ferree and Barbash 2009; Sawamura et al. 1993a; Sawamura et al. 1993b) suggest that uniparentally inherited genetic factors play an important role in explaining differences in postzygotic RI between reciprocal crosses. These can include effects of maternally transmitted symbionts like Wolbachia bacteria on RI (Williamson and Ehrman 1967; Miller et al. 2010), although this is likely rare (Cooper et al. 2017). Parent‐of‐origin effects are common in taxa with placentas. Thus, the relative frequency of asymmetric RI might differ between groups that have a placenta and imprinting (e.g. mammals, angiosperms) and groups that do not (e.g. birds). Asymmetrical RI could have important consequences for how speciation is completed. Asymmetric gene exchange might reduce the likelihood of reinforcement and the likelihood of introgression (Servedio and Kirkpatrick 1997). Studies on the relationship between genetic distance and RI asymmetry are rare. As divergence accrues, asymmetry in RI increases in centrarchid fishes (Bolnick and Near 2005). There is no relationship in the asymmetry in ability to find food in Drosophila hybrids (Turissini et al. 2017) or in the asymmetry of isolation in Jaltomata nightshades (Kostyun and Moyle 2017). In general, even though asymmetries in RI are common and genetic models have been extensively researched, the consequences of Darwin's Corollary in speciation remain largely unknown.

CONCLUSIONS

The seminal work of C&O (1989) demonstrated the power and utility of the comparative approach for understanding general patterns of RI, but there are limitations, including the inability of these analyses to reveal which barriers contribute most to speciation. The spirit of several analyses in C&O (1989) was to determine “which type of isolation is most important in reducing gene flow between incipient species.” Decades of cataloguing species differences and identifying traits that reduce gene flow strongly suggest that different traits function jointly to maintain species boundaries. These traits might evolve simultaneously and affect the rates of evolution of other traits (e.g., Langerhans et al. 2007). The existence of reinforcement itself confirms the complex interaction between different traits, as prezygotic RI may evolve as a byproduct of selection against maladaptive hybridization.

Since C&O (1989), hundreds of studies have described the increase of RI along divergence. Still today, there is not a unified systematic understanding of how RI accumulates in phylogenetic trees, and the infusion of a fully quantitative phylogenetic background to the study of RI remains in its infancy. Comparative approaches to study speciation remain relevant and will continue to inform how species form and persist in nature. We are optimistic about the future of speciation research, including the continued influence of C&O (1989) on the field.

AUTHOR CONTRIBUTIONS

D.R. Matute and B.S. Cooper wrote the article.

Associate Editor: T. Chapman

Handling Editor: T. Chapman

ACKNOWLEDGMENTS

We thank M. Turelli, J. M. Good, and members of the Matute lab for comments on earlier versions of this manuscript. National Institute of General Medical Sciences funded the authors under Award Number R01GM121750 to D.R.M. and R35GM124701 to B.S.C. The authors have no conflict of interests. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.

LITERATURE CITED

  1. Abzhanov, A. , Protas M., Grant B. R., Grant P. R., and Tabin C. J.. 2004. Bmp4 and morphological variation of beaks in Darwin's finches. Science 305:1462–1465. [DOI] [PubMed] [Google Scholar]
  2. Arnegard, M. E. , McIntyre P. B., Harmon L. J., Zelditch M. L., Crampton W. G., Davis J. K., Sullivan J. P., Lavoué S., and Hopkins C. D., 2010. Sexual signal evolution outpaces ecological divergence during electric fish species radiation. Am. Nat 176:335–356. [DOI] [PubMed] [Google Scholar]
  3. Arnegard, M. E. , McGee M. D., Matthews B., Marchinko K. B., Conte G. L., Kabir S., Bedford N., Bergek S., Chan Y. F., and Jones F. C.. 2014. Genetics of ecological divergence during speciation. Nature 511:307–311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Arrieta, R. S. , Lijtmaer D. A., and Tubaro P. L.. 2013. Evolution of postzygotic reproductive isolation in galliform birds: analysis of first and second hybrid generations and backcrosses. Biol. J. Linn. Soc 110:528–542. [Google Scholar]
  5. Ayala, F. J. , Tracey M. L., Hedgecock D., and Richmond R. C.. 1974. Genetic differentiation during the speciation process in Drosophila . Evolution 28:576–592. [DOI] [PubMed] [Google Scholar]
  6. Barbash, D. A. , and Ashburner M.. 2003. A novel system of fertility rescue in Drosophila hybrids reveals a link between hybrid lethality and female sterility. Genetics 163:217‐226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Barnard‐Kubow, K. B. , and Galloway L. F.. 2017. Variation in reproductive isolation across a species range. Ecol. Evol 7:9347–9357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bendall, E. E. , Vertacnik K. L., and Linnen C. R.. 2017. Oviposition traits generate extrinsic postzygotic isolation between two pine sawfly species. BMC Evol. Biol 17:26. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Blanckaert, A. , and Bank C.. 2018. In search of the Goldilocks zone for hybrid speciation. PLos Genet 14:e1007613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Blair, W. F. 1955. Mating call and stage of speciation in the Microhyla olivacea‐. carolinensis complex. Evolution 9:469–480. [Google Scholar]
  11. Bock, I. R. 1984. Interspecific Hybridization in the Genus Drosophila . Pp. 41–70 in Hecht M. K., Wallace B., and Prance G. T., eds. Evolutionary Biology: Volume 18. Springer; US, Boston, MA. [Google Scholar]
  12. Bolnick, D. I. , and Near T. J.. 2005. Tempo of hybrid inviability in centrarchid fishes (Teleostei: Centrarchidae). Evolution 59:1754‐1767. [PubMed] [Google Scholar]
  13. Bothwell, E. , Montgomerie R., Lougheed S. C., and Martin P. R.. 2015. Closely related species of birds differ more in body size when their ranges overlap—in warm, but not cool, climates. Evolution 69:1701–1712. [DOI] [PubMed] [Google Scholar]
  14. Bracewell, R. R. , Bentz B. J., Sullivan B. T., and Good J. M.. 2017. Rapid neo‐sex chromosome evolution and incipient speciation in a major forest pest. Nat. Commun 8:1–14. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Brekke, T. D. , and Good J. M.. 2014. Parent‐of‐origin growth effects and the evolution of hybrid inviability in dwarf hamsters. Evolution 68:3134–3148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Buerkle, C. A. , Morris R. J., Asmussen M. A., and Rieseberg L. H.. 2000. The likelihood of homoploid hybrid speciation. Heredity 4:441‐451. [DOI] [PubMed] [Google Scholar]
  17. Bundus, J. D. , Wang D., and Cutter A. D.. 2018. Genetic basis to hybrid inviability is more complex than hybrid male sterility in Caenorhabditis nematodes. Heredity 121:169–182. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Burton, R. S. 1990. Hybrid breakdown in developmental time in the Copepod Tigriopus californicus . Evolution 44:1814–1822. [DOI] [PubMed] [Google Scholar]
  19. Butlin, R. 1987. A new approach to sympatric speciation. Trends Ecol. Evol 2:310–311. [DOI] [PubMed] [Google Scholar]
  20. Butlin, R. K. 2010. Population genomics and speciation. Genetica 138:409–418. [DOI] [PubMed] [Google Scholar]
  21. Campagna, L. , Benites P., Lougheed S. C., Lijtmaer D. A., Di Giacomo A. S., Eaton M. D., and Tubaro P. L.. 2012. Rapid phenotypic evolution during incipient speciation in a continental avian radiation. Proc. R. Soc. B 279:1847–1856. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Campbell, C. R. , Poelstra J. W., and Yoder A. D.. 2018. What is speciation genomics? The roles of ecology, gene flow, and genomic architecture in the formation of species. Biol. J. Linn. Soc 124:561–583. [Google Scholar]
  23. Castillo, D. M. , and Moyle L. C.. 2019. Conspecific sperm precedence is reinforced, but postcopulatory sexual selection weakened, in sympatric populations of Drosophila . Proc. R. Soc. B 286:20182535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Chapman, M. A. , and Burke J. M.. 2007. Genetic divergence and hybrid speciation. Evolution 61:1773–1780. [DOI] [PubMed] [Google Scholar]
  25. Charistianson, S. J. , Swallow J. G., and Wilkinson G. S.. 2005. Rapid evolution of postzygotic reproductive isolation in stalk‐eyed flies. Evolution 59:849–857. [PubMed] [Google Scholar]
  26. Christie, K. , and Strauss S. Y.. 2018. Along the speciation continuum: Quantifying intrinsic and extrinsic isolating barriers across five million years of evolutionary divergence in California jewelflowers. Evolution 72:1063–1079. [DOI] [PubMed] [Google Scholar]
  27. Clark, M. E. , O'Hara F. P., Chawla A., and Werren J. H.. 2010. Behavioral and spermatogenic hybrid male breakdown in Nasonia . Heredity 104:289–301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Comeault, A. A. 2018. The genomic and ecological context of hybridization affects the probability that symmetrical incompatibilities drive hybrid speciation. Ecology and Evolution 5:2926–2937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Comeault, A. A. , and Matute D. R.. 2018. Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation. Proc. Natl. Acad. Sci. U. S. A 115:9761–9766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Cooper, B. S. , Ginsberg P. S., Turelli M., and Matute D. R.. 2017. Wolbachia in the Drosophila yakuba complex: Pervasive frequency variation and weak cytoplasmic incompatibility, but no apparent effect on reproductive isolation. Genetics 205:333–351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Cooper, B. S. , Sedghifar A., Nash W. T., Comeault A. A., and Matute D. R.. 2018. A maladaptive combination of traits contributes to the maintenance of a Drosophila hybrid zone. Curr. Biol 28:2940–2947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Coughlan, J. M. , Brown M. W., and Willis J. H.. 2020. Patterns of hybrid seed inviability in the Mimulus guttatus sp. complex reveal a potential role of parental conflict in reproductive isolation. Curr. Biol 30:83‐93.e5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Coughlan, J. M. , and Matute D. R.. 2020. The importance of intrinsic postzygotic barriers throughout the speciation process. Philosophical Transactions of the Royal Society B: Biological Sciences 375:20190533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Coyne, J. A. , 1974. The evolutionary origin of hybrid inviability. Evolution 28:505‐506. [DOI] [PubMed] [Google Scholar]
  35. Coyne, J. A. 1989. Genetics of sexual isolation between two sibling species, Drosophila simulans and Drosophila mauritiana . Proc. Natl. Acad. Sci. U. S. A 86:5464–5468. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Coyne, J. A. , and Orr H. A., 1989. Patterns of speciation in Drosophila . Evolution 43:362–381. [DOI] [PubMed] [Google Scholar]
  37. Coyne, J. A. , and Orr H. A.. 1997. “Patterns of Speciation in Drosophila” Revisited. Evolution 51:295‐303. [DOI] [PubMed] [Google Scholar]
  38. Coyne, J. A. , and Orr H. A.. 2004. Speciation. Sunderland, MA. Sinauer Associates. [Google Scholar]
  39. Cruickshank, T. , and Wade M. J.. 2008. Microevolutionary support for a developmental hourglass: gene expression patterns shape sequence variation and divergence in Drosophila . Evol. Dev 10:583–590. [DOI] [PubMed] [Google Scholar]
  40. Cutter, A. D. , and Bundus J. D.. 2020. Speciation and the developmental alarm clock. eLife 9:e56276. eLife Sciences Publications, Ltd. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Darwin, C. 1859. On the origin of species by means of natural selection, or preservation of favoured races in the struggle for life. John Murray, London. [PMC free article] [PubMed]
  42. Delmore, K. E. , and Irwin D. E.. 2014. Hybrid songbirds employ intermediate routes in a migratory divide. Ecology Letters 17:1211–1218. [DOI] [PubMed] [Google Scholar]
  43. Delph, L. F. , and Demuth J. P.. 2016. Haldane's rule: genetic bases and their empirical support. J. Hered 107:383–391.Oxford University Press US. [DOI] [PubMed] [Google Scholar]
  44. Dobzhansky, T. 1937. Genetic nature of species differences. Am. Nat 71:404–420. [Google Scholar]
  45. Dobzhansky, T. , 1940. Speciation as a stage in evolutionary divergence. Am. Nat 74, pp.312‐321. [Google Scholar]
  46. Dobzhansky, T. , and Spassky B.. 1959. Drosophila paulistorum, a cluster of species in statu nascendi*. Proc. Natl. Acad. Sci. U. S. A 45:419–428. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Edmands, S. 2002. Does parental divergence predict reproductive compatibility? Trends Ecol. Evol 17:520–527. [Google Scholar]
  48. Ehrman, L. 1965. Direct observation of sexual isolation between allopatric and between sympatric strains of the different Drosophila paulistorum races. Evolution 459–464. [Google Scholar]
  49. Eo, S. H. , and DeWoody J. A., 2010. Evolutionary rates of mitochondrial genomes correspond to diversification rates and to contemporary species richness in birds and reptiles. Proc. Natl. Acad. Sci. U. S. A 277:3587–3592. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Etges, W. J. 1998. Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. IV. Correlated responses in behavioral isolation to artificial selection on a life‐history trait. Am. Nat 152:129–144. [DOI] [PubMed] [Google Scholar]
  51. Felsenstein, J. 1985. Phylogenies and the Comparative Method. Am. Nat 125:1–15.The University of Chicago Press. [Google Scholar]
  52. Ferree, P. M. , and Barbash D. A.. 2009. Species‐specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila . PLoS Biol 7:e1000234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Fitzpatrick B. M. 2002. Molecular correlates of reproductive isolation. Evolution 56:191–198. [DOI] [PubMed] [Google Scholar]
  54. Fitzpatrick, B. M. 2004. Rates of evolution of hybrid inviability in birds and mammals. Evolution 58:1865–1870. [DOI] [PubMed] [Google Scholar]
  55. Fouquette, Jr, M. J. 1975. Speciation in chorus frogs. I. Reproductive character displacement in the Pseudacris nigrita complex. Syst. Biol 24:16–23.Society of Systematic Zoology. [Google Scholar]
  56. Funk, D. J. , Nosil P., and Etges W. J.. 2006. Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proc. Natl. Acad. Sci. U. S. A 103:3209–3213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Giraud, T. , and Gourbière S.. 2012. The tempo and modes of evolution of reproductive isolation in fungi. Heredity 109:204–214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Gleason, J. M. , and Ritchie M. G.. 1998. Evolution of courtship song and reproductive isolation in the Drosophila willistoni species complex: Do sexual signals diverge the most quickly? Evolution 52:1493–1500. [DOI] [PubMed] [Google Scholar]
  59. Good, J. M. , Dean M. D., and Nachman M. W.. 2008. A complex genetic basis to x‐linked hybrid male sterility between two species of house mice. Genetics 179:2213–2228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Gottsberger, B. , and Mayer F.. 2007. Behavioral sterility of hybrid males in acoustically communicating grasshoppers (Acrididae, Gomphocerinae). J Comp Physiol A 193:703–714. [DOI] [PubMed] [Google Scholar]
  61. Gourbière, S. , and Mallet J.. 2010. Are species real? The shape of the species boundary with exponential failure, reinforcement, and the “missing snowball. Evolution 64:1–24. [DOI] [PubMed] [Google Scholar]
  62. Grant, V. 1994. Modes and origins of mechanical and ethological isolation in angiosperms. Proc. Natl. Acad. Sci. U. S. A 91:3–10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Gray, A. P. 1972. Mammalian hybrids: A check‐list with bibliography,. 2nd Edition. Commonwealth Agricultural Bureaux, Slough. [Google Scholar]
  64. Gross, B. L. , and Rieseberg L. H.. 2005. The ecological genetics of homoploid hybrid speciation. J. Hered 96:241–252. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Grossenbacher, D. L. , and Whittall J. B.. 2011. Increased floral divergence in sympatric monkeyflowers. Evolution 65:2712–2718. [DOI] [PubMed] [Google Scholar]
  66. Haldane, J. B. S. 1922. Sex ratio and unisexual sterility in hybrid animals. J. Genet 12:101–109.Springer. [Google Scholar]
  67. Hamlin, J. A. P. , Hibbins M. S., and Moyle L. C.. 2020. Assessing biological factors affecting postspeciation introgression. Evol. Lett 4:137‐154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Harvey, M. G. , Singhal S., and Rabosky D. L.. 2019. Beyond reproductive isolation: Demographic controls on the speciation process. Annu. Rev. Ecol. Evol. Syst 50:75–95. [Google Scholar]
  69. Higgie, M. , Chenoweth S., and Blows M. W.. 2000. Natural selection and the reinforcement of mate recognition. Science 290:519–521. [DOI] [PubMed] [Google Scholar]
  70. Hooper, D. M. , and Price T. D.. 2017. Chromosomal inversion differences correlate with range overlap in passerine birds. Nat. Ecol. Evol 1:1526–1534. [DOI] [PubMed] [Google Scholar]
  71. Hooper, D. M. , Griffith S. C., and Price T. D., 2019. Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone. Mol. Ecol 28:1246–1262. [DOI] [PubMed] [Google Scholar]
  72. Hopkins, R. 2013. Reinforcement in plants. New Phytol. 4:1095‐1103. [DOI] [PubMed] [Google Scholar]
  73. Hopkins, R. , and Rausher M. D.. 2012. Pollinator‐mediated selection on flower color allele drives reinforcement. Science 335:1090–1092. [DOI] [PubMed] [Google Scholar]
  74. Howard, D. J. 1999. Conspecific sperm and pollen precedence and speciation. Annu. Rev. Ecol. Syst 30:109–132. [Google Scholar]
  75. Hudson, E. J. , and Price T. D.. 2014. Pervasive reinforcement and the role of sexual selection in biological speciation. J. Hered. 105:821–833. [DOI] [PubMed] [Google Scholar]
  76. Huey, R. B. , and Pianka E. R.. 1981. Ecological consequences of foraging mode. Ecology 62:991–999. [Google Scholar]
  77. Huey, R. B. , Garland T. Jr and Turelli M., 2019. Revisiting a key innovation in evolutionary biology: Felsenstein's “phylogenies and the comparative method. Am. Nat 193:755–772. [DOI] [PubMed] [Google Scholar]
  78. Ishikawa, R. , Ohnishi T., Kinoshita Y., Eiguchi M., Kurata N., and Kinoshita T.. 2011. Rice interspecies hybrids show precocious or delayed developmental transitions in the endosperm without change to the rate of syncytial nuclear division. Plant J 65:798–806. [DOI] [PubMed] [Google Scholar]
  79. Irwin, D. E. , 2020. Assortative mating in hybrid zones is remarkably ineffective in promoting speciation. Am. Nat 195:E150‐E167. [DOI] [PubMed] [Google Scholar]
  80. Jablonski, D. , Huang S., Roy K., and Valentine J. W.. 2017. Shaping the latitudinal diversity gradient: new perspectives from a synthesis of paleobiology and biogeography. Am. Nat 189:1–12. [DOI] [PubMed] [Google Scholar]
  81. Janicke, T. , Marie‐Orleach L., Aubier T. G., Perrier C., and Morrow E. H.. 2019. Assortative mating in animals and its role for speciation. Am. Nat 194:865–875. [DOI] [PubMed] [Google Scholar]
  82. Jewell, C. , Papineau A. D., Freyre R., and Moyle L. C.. 2012. Patterns of reproductive isolation in Nolana (Chilean Bellflower). Evolution 66:2628–2636. [DOI] [PubMed] [Google Scholar]
  83. Jiggins, C. D. , Linares M., Naisbit R. E., Salazar C., Yang Z. H., and Mallet J., 2001. Sex‐linked hybrid sterility in a butterfly. Evolution 55:1631–1638. [DOI] [PubMed] [Google Scholar]
  84. Johnson, N. A. 2010. Hybrid incompatibility genes: remnants of a genomic battlefield? Trends Genet 26:317–325. [DOI] [PubMed] [Google Scholar]
  85. Johnson, N. A. , and Lachance J., 2012. The genetics of sex chromosomes: evolution and implications for hybrid incompatibility. Ann. N. Y. Acad. Sci 1256:E1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Kaiser, V. B. , and Bachtrog D.. 2010. Evolution of sex chromosomes in insects. Annu. Rev. Genet 44:91–112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Kalinka, A. T. , Varga K. M., Gerrard D. T., Preibisch S., Corcoran D. L., Jarrells J., Ohler U., Bergman C. M., and Tomancak P.. 2010. Gene expression divergence recapitulates the developmental hourglass model. Nature 468:811–814. [DOI] [PubMed] [Google Scholar]
  88. Kitano, J. , and Peichel C. L.. 2012. Turnover of sex chromosomes and speciation in fishes. Environ. Biol. Fishes 94:549–558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Kitano, J. , Ross J. A., Mori S., Kume M., Jones F. C., Chan Y. F., Absher D. M., Grimwood J., Schmutz J., Myers R. M., et al. 2009. A role for a neo‐sex chromosome in stickleback speciation. Nature 461:1079–1083. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Koevoets, T. , and Beukeboom L. W.. 2009. Genetics of postzygotic isolation and Haldane's rule in haplodiploids. Heredity 102:16–23. [DOI] [PubMed] [Google Scholar]
  91. Koopman, K. F. 1950. Natural selection for reproductive isolation between Drosophila pseudoobscura and Drosophila persimilis . Evolution 4:135–148. [Google Scholar]
  92. Kost, S. , Heckel D. G., Yoshido A., Marec F., and Groot A. T.. 2016. A Z‐linked sterility locus causes sexual abstinence in hybrid females and facilitates speciation in Spodoptera frugiperda . Evolution 70:1418–1427. [DOI] [PubMed] [Google Scholar]
  93. Kostyun, J. L. , and Moyle L. C.. 2017. Multiple strong postmating and intrinsic postzygotic reproductive barriers isolate florally diverse species of Jaltomata (Solanaceae). Evolution 71:1556–1571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Kronforst, M. R. , Hansen M. E. B., Crawford N. G., Gallant J. R., Zhang W., Kulathinal R. J., Kapan D. D., and Mullen S. P.. 2013. Hybridization reveals the evolving genomic architecture of speciation. Cell Rep 5:666–677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Lackey, A. C. R. , and Boughman J. W.. 2017. Evolution of reproductive isolation in stickleback fish. Evolution 71:357–372. [DOI] [PubMed] [Google Scholar]
  96. Langerhans, R. B. , Gifford M. E., and Joseph E. O.. 2007. Ecological speciation in Gambusia fishes. Evolution 61:2056–2074. [DOI] [PubMed] [Google Scholar]
  97. Larson, E. L. , Vanderpool D., Sarver B. A. J., Callahan C., Keeble S., Provencio L. L., Kessler M. D., Stewart V., Nordquist E., Dean M. D., et al. 2018. The evolution of polymorphic hybrid incompatibilities in house mice. Genetics 209:845–859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Laurie, C. C. 1997. The weaker sex is heterogametic: 75 years of Haldane's Rule. Genetics 147:937–951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Lawson, A. M. , and Weir J. T.. 2014. Latitudinal gradients in climatic‐niche evolution accelerate trait evolution at high latitudes. Ecology Letters 17:1427–1436. [DOI] [PubMed] [Google Scholar]
  100. Lemmon, E. M. , and Lemmon A. R.. 2010. Reinforcement in chorus frogs: lifetime fitness estimates including intrinsic natural selection and sexual selection against hybrids. Evolution 64:1748–1761. [DOI] [PubMed] [Google Scholar]
  101. Levin, D. A. 1985. Reproductive character displacement in Phlox. Evolution 39:1275–1281. [DOI] [PubMed] [Google Scholar]
  102. Lijtmaer, D. A. , Mahler B., and Tubaro P. L.. 2003. Hybridization and postzygotic isolation patterns in pigeons and doves. Evolution 57:1411–1418. [DOI] [PubMed] [Google Scholar]
  103. Lima, T. G. 2014. Higher levels of sex chromosome heteromorphism are associated with markedly stronger reproductive isolation. Nat. Commun 5:4743. [DOI] [PubMed] [Google Scholar]
  104. Linn, C. E. , Dambroski H. R., Feder J. L., Berlocher S. H., Nojima S., and Roelofs W. L.. 2004. Postzygotic isolating factor in sympatric speciation in Rhagoletis flies: Reduced response of hybrids to parental host‐fruit odors. Proc. Natl. Acad. Sci. U. S. A 101:17753–17758. [DOI] [PMC free article] [PubMed] [Google Scholar]
  105. Liou, L. W. , and Price T. D.. 1994. Speciation by reinforcement of premating isolation. Evolution 48:1451. [DOI] [PubMed] [Google Scholar]
  106. Littlejohn, M. J. 1965. Premating isolation in the Hyla ewingi complex (Anura: Hylidae). Evolution 234–243. [DOI] [PubMed] [Google Scholar]
  107. Liu, J. , Frochaux M., Gardeux V., Deplancke B., and Robinson‐Rechavi M.. 2019. Selection against expression noise explains the origin of the hourglass pattern of Evo‐Devo. bioRxiv 700997. [Google Scholar]
  108. Loftus‐Hills, J. J. 1975. The evidence for reproductive character displacement between the toads Bufo americanus and B. woodhousii fowleri . Evolution 29:368 Cambridge Univ. Press. [DOI] [PubMed] [Google Scholar]
  109. Lorch, P. D. , and Servedio M. R.. 2005. Postmating‐prezygotic isolation is not an important source of selection for reinforcement within and between species in Drosophila pseudoobscura and D. persimilis . Evolution 59:1039–1045. [PubMed] [Google Scholar]
  110. Lowry, D. B. , Modliszewski J. L., Wright K. M., Wu C. A., and Willis J. H.. 2008. The strength and genetic basis of reproductive isolating barriers in flowering plants. Philos. Trans. R. Soc. B: Biol. Sci 363:3009–3021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  111. MacIntyre, R. J. , and Collier G. E.. 1986. Protein evolution in the genus Drosophila . The Genetics and Biology of Drosophila 3:39–146.Academic Press London. [Google Scholar]
  112. Mallarino, R. , and Abzhanov A.. 2012. Paths less traveled: Evo‐devo approaches to investigating animal morphological Evolution Annu. Rev. Cell Dev. Biol 28:743–763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  113. Mallet, J. 2007. Hybrid speciation. Nature 446:279–283. [DOI] [PubMed] [Google Scholar]
  114. Mallet, J. 2004. Perspectives Poulton, Wallace and Jordan: how discoveries in Papilio butterflies led to a new species concept 100 years ago. Syst. Biodivers 1, pp. 441‐452. [Google Scholar]
  115. Malone, J. H. , and Fontenot B. E.. 2008. Patterns of reproductive isolation in toads. PLoS One 3:e3900. [DOI] [PMC free article] [PubMed] [Google Scholar]
  116. Markow, T. A. 1981. Courtship behavior and control of reproductive isolation between Drosophila mojavensis and Drosophila arizonensis . Evolution 1022–1026. [DOI] [PubMed] [Google Scholar]
  117. Marques, D. A. , Meier J. I., and Seehausen O.. 2019. A combinatorial view on speciation and adaptive radiation. Trends Ecol. Evol 34:531–544. [DOI] [PubMed] [Google Scholar]
  118. Martin, P. R. , Montgomerie R., and Lougheed S. C.. 2015. Color patterns of closely related bird species are more divergent at intermediate levels of breeding‐range sympatry. Am. Nat 185:443–451. [DOI] [PubMed] [Google Scholar]
  119. Masly, J. P. , and Presgraves D. C.. 2007. High‐resolution genome‐wide dissection of the two rules of speciation in Drosophila. PLoS Biol 5:e243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. Matute, D. R. 2010a. Reinforcement can overcome gene flow during speciation in Drosophila . Curr. Biol 20:2229–2233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. Matute, D. R. 2010b. Reinforcement of gametic isolation in Drosophila . PLoS Biol 8:e1000341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  122. Matute, D. R. , Butler I. A., Turissini D. A., and Coyne J. A.. 2010. A test of the snowball theory for the rate of evolution of hybrid incompatibilities. Science 329:1518–1521. [DOI] [PubMed] [Google Scholar]
  123. Matute, D. R. , and Coyne J. A.. 2010. Intrinsic reproductive isolation between two sister species of Drosophila . Evolution 64:903–920. [DOI] [PubMed] [Google Scholar]
  124. Matute, D. R. , and Gavin‐Smyth J.. 2014. Fine mapping of dominant x‐linked incompatibility alleles in Drosophila hybrids. PLos Genet 10:e1004270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  125. Matute, D. R. , Gavin‐Smyth J., and Liu G.. 2014. Variable post‐zygotic isolation in Drosophila melanogaster/D. simulans hybrids. J. Evol. Biol 27:1691‐1705. [DOI] [PubMed] [Google Scholar]
  126. Mayr, E. 1963. Animal species and Evolution. Cambridge, MA, Belknap Press of Harvard University Press. [Google Scholar]
  127. McBride, C. S. , and Singer M. C.. 2010. Field studies reveal strong postmating isolation between ecologically divergent butterfly populations. PLoS Biol 8:e1000529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  128. McQuillan, M. A. , Roth T. C., Huynh A. V., and Rice A. M.. 2018. Hybrid chickadees are deficient in learning and memory. Evolution 72:1155–1164. [DOI] [PubMed] [Google Scholar]
  129. Meier, J. I. , Marques D. A., Mwaiko S., Wagner C. E., Excoffier L., and Seehausen O.. 2017. Ancient hybridization fuels rapid cichlid fish adaptive radiations. Nat. Commun 8:1–11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  130. Meiklejohn, C. D. , and Tao Y.. 2010. Genetic conflict and sex chromosome Evolution Trends Ecol. Evol 25:215–223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  131. Mendelson, T. C. 2003. Sexual isolation evolves faster than hybrid inviability in a diverse and sexually dimorphic genus of fish (Percidae: Etheostoma). Evolution 57:317–327. [DOI] [PubMed] [Google Scholar]
  132. Mendelson, T. C. , Inouye B. D., and Rausher M. D.. 2004. Quantifying patterns in the evolution of reproductive isolation. Evolution 58:1424–1433. [DOI] [PubMed] [Google Scholar]
  133. Mendelson, T. C. , Gumm J. M., Martin M. D., and Ciccotto P. J.. 2018. Preference for conspecifics evolves earlier in males than females in a sexually dimorphic radiation of fishes. Evolution 72:337–347. [DOI] [PubMed] [Google Scholar]
  134. Miller, W. J. , Ehrman L., and Schneider D.. 2010. Infectious speciation revisited: impact of symbiont‐depletion on female fitness and mating behavior of Drosophila paulistorum. PLoS Pathog 6:e1001214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  135. Moran, R. L. , Zhou M., Catchen J. M., and Fuller R. C., 2017. Male and female contributions to behavioral isolation in darters as a function of genetic distance and color distance. Evolution 71:2428–2444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  136. Moran, P. A. , Hunt J., Mitchell C., Ritchie M. G., and Bailey N. W., 2020. Sexual selection and population divergence III: Interspecific and intraspecific variation in mating signals. J. Evol. Biol 33:990–1005. [DOI] [PubMed] [Google Scholar]
  137. Moyle, L. C. , and Nakazato T.. 2010. Hybrid incompatibility “snowballs” between Solanum species. Science 329:1521–1523. [DOI] [PubMed] [Google Scholar]
  138. Moyle, L. C. , Olson M. S., and Tiffin P.. 2004. Patterns of reproductive isolation in three angiosperm genera. Evolution 58:1195‐1208. [DOI] [PubMed] [Google Scholar]
  139. Moyle, L. C. , and Payseur B. A., 2009. Reproductive isolation grows on trees. Trends Ecol. Evol 24:591–598. [DOI] [PubMed] [Google Scholar]
  140. Muirhead, C. A. , and Presgraves D. C.. 2016. Hybrid incompatibilities, local adaptation, and the genomic distribution of natural introgression between species. Am. Nat 187:249–261. [DOI] [PubMed] [Google Scholar]
  141. Naisbit, R. E. , Jiggins C. D., and Mallet J.. 2001. Disruptive sexual selection against hybrids contributes to speciation between Heliconius cydno and Heliconius melpomene . Proc. Roy. Soc. B 268:1849–1854. [DOI] [PMC free article] [PubMed] [Google Scholar]
  142. Niet, T.aner. , Johnson S. D., and Linder H. P.. 2006. Macroevolutionary data suggest a role for reinforcement in pollination system shifts. Evolution 60:1596–1601. [DOI] [PubMed] [Google Scholar]
  143. Nieto Feliner, G. , Álvarez I., Fuertes‐Aguilar J., Heuertz M., Marques I., Moharrek F., Piñeiro R., Riina R., Rosselló J. A., Soltis P. S., et al. 2017. Is homoploid hybrid speciation that rare? An empiricist's view. Heredity 118:513–516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  144. Noor, M. A. 1997. How often does sympatry affect sexual isolation in Drosophila? Am. Nat 149:1156–1163. [DOI] [PubMed] [Google Scholar]
  145. Noor, M. A. 1995. Speciation driven by natural selection in Drosophila . Nature 375:674–675. [DOI] [PubMed] [Google Scholar]
  146. Nosil, P. , 2008. Speciation with gene flow could be common. Mol. Ecol 17:2103–2106. [DOI] [PubMed] [Google Scholar]
  147. Nosil, P. , and Hohenlohe P. A., 2012. Dimensionality of sexual isolation during reinforcement and ecological speciation in Timema cristinae stick insects. Evol. Ecol. Res 14:467–485. [Google Scholar]
  148. Nosil, P. 2013. Degree of sympatry affects reinforcement in Drosophila . Evolution 67:868–872. [DOI] [PubMed] [Google Scholar]
  149. Nosil, P. 2012. Ecological Speciation. Oxford, Oxford University Press. [Google Scholar]
  150. O'Meara, B. C. 2012. Evolutionary inferences from phylogenies: A review of methods. Annu. Rev. Ecol. Evol. Syst 43:267–285. [Google Scholar]
  151. Oneal, E. , Willis J. H., and Franks R. G.. 2016. Disruption of endosperm development is a major cause of hybrid seed inviability between Mimulus guttatus and Mimulus nudatus . New Phytol 210:1107–1120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  152. Orr, H. A. 1997. Haldane's Rule. Annual Review of Ecology and Systematics 28:195–218. [DOI] [PubMed] [Google Scholar]
  153. Orr, H. A. 1993. Haldane's rule has multiple genetic causes. Nature 361:532‐533. [DOI] [PubMed] [Google Scholar]
  154. Orr, H. A. 2005. The genetic basis of reproductive isolation: Insights from Drosophila . Proc. Natl. Acad. Sci. U. S. A 102:6522–6526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  155. Orr, H. A. 1995. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139:1805–1813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  156. Orr, H. A. , Masly J. P., and Phadnis N.. 2007. Speciation in Drosophila: From phenotypes to molecules. J. Hered 98:103–110. [DOI] [PubMed] [Google Scholar]
  157. Orr, H. A. , and Presgraves D. C.. 2000. Speciation by postzygotic isolation: Forces, genes and molecules. Bioessays 22:1085–1094. [DOI] [PubMed] [Google Scholar]
  158. Paterson, H. E. H. 1978. More evidence against speciation by reinforcement. S. Afr. J. Sci 74:369. [Google Scholar]
  159. Paun, O. , Forest F., Fay M. F., and Chase M. W.. 2009. Hybrid speciation in angiosperms: parental divergence drives ploidy. New Phytol 182:507–518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  160. Pennell, M. W. , and Harmon L. J.. 2013. An integrative view of phylogenetic comparative methods: connections to population genetics, community ecology, and paleobiology: Integrative comparative methods. Ann. N.Y. Acad. Sci 1289:90–105. [DOI] [PubMed] [Google Scholar]
  161. Pereira, R. J. , Monahan W. B., and Wake D. B.. 2011. Predictors for reproductive isolation in a ring species complex following genetic and ecological divergence. BMC Evol. Biol 11:194. [DOI] [PMC free article] [PubMed] [Google Scholar]
  162. Phadnis, N. , Baker E. P., Cooper J. C., Frizzell K. A., Hsieh E., de la Cruz A. F. A., Shendure J., Kitzman J. O., and Malik H. S.. 2015. An essential cell cycle regulation gene causes hybrid inviability in Drosophila . Science (New York, N.Y.) 350:1552–1555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  163. Phillips, B. C. , and Edmands S., 2012. Does the speciation clock tick more slowly in the absence of heteromorphic sex chromosomes?. Bioessays 34:166–169. [DOI] [PubMed] [Google Scholar]
  164. Poulton, E. B. , 1904. What is a species?(Presidential address to the Entomological Society of London). In Proceedings of the Entomological Society London  (pp. 1889–1907).
  165. Prager, E. M. , and Wilson A. C.. 1975. Slow evolutionary loss of the potential for interspecific hybridization in birds: a manifestation of slow regulatory Evolution Proc. Natl. Acad. Sci. U. S. A 72:200–204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  166. Presgraves, D. C. 2018. Evaluating genomic signatures of “the large X‐effect” during complex speciation. Mol. Ecol 27:3822–3830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  167. Presgraves, D. C. 2002. Patterns of Postzygotic Isolation in Lepidoptera. Evolution 56:1168–1183. [DOI] [PubMed] [Google Scholar]
  168. Presgraves, D. C. 2008. Sex chromosomes and speciation in Drosophila . Trends Genet 24:336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  169. Presgraves, D. C. , and Orr H. A., 1998. Haldane's rule in taxa lacking a hemizygous X. Science 282:952–954. [DOI] [PubMed] [Google Scholar]
  170. Price, T. D. , and Bouvier M. M.. 2002. The evolution of F1 postzygotic incompatibilities in birds. Evolution 56:2083–2089. [PubMed] [Google Scholar]
  171. Rabosky, D. L. 2016. Reproductive isolation and the causes of speciation rate variation in nature. Biol. J. Linn. Soc 118:13–25. [Google Scholar]
  172. Rabosky, D. L. , and Matute D. R.. 2013. Macroevolutionary speciation rates are decoupled from the evolution of intrinsic reproductive isolation in Drosophila and birds. Proc. Natl. Acad. Sci. U. S. A 110:15354–15359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  173. Rebernig, C. A. , Lafon‐Placette C., Hatorangan M. R., Slotte T., and Köhler C.. 2015. Non‐reciprocal interspecies hybridization barriers in the Capsella genus are established in the endosperm. PLos Genet 11:e1005295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  174. Rice, A. M. , Rudh A., Ellegren H., and Qvarnström A.. 2011. A guide to the genomics of ecological speciation in natural animal populations. Ecology Letters 14:9–18. [DOI] [PubMed] [Google Scholar]
  175. Rice, W. R. , and Hostert E. E.. 1993. Laboratory experiments on speciation: what have we learned in 40 years? Evolution 47:1637–1653. [DOI] [PubMed] [Google Scholar]
  176. Ritchie, M. G. , and Gleason J. M., 1995. Rapid evolution of courtship song pattern in Drosophila willistoni sibling species. J. Evol. Biol 8:463–479. [Google Scholar]
  177. Rosenblum, E. B. , Sarver B. A. J., Brown J. W., Des Roches S., Hardwick K. M., Hether T. D., Eastman J. M., Pennell M. W., and Harmon L. J.. 2012. Goldilocks meets Santa Rosalia: An ephemeral speciation model explains patterns of diversification across time scales. Evol. Biol 39:255–261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  178. Roux, C. , Fraïsse C., Romiguier J., Anciaux Y., Galtier N., and Bierne N.. 2016. Shedding light on the grey zone of speciation along a continuum of genomic divergence. PLoS Biol 14:e2000234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  179. Russell, S. T. , 2003. January. Evolution of intrinsic post‐zygotic reproductive isolation in fish. In Annales Zoologici Fennici 40:321–329. [Google Scholar]
  180. Sánchez, L. , and Santamaria P.. 1997. Reproductive isolation and morphogenetic evolution in Drosophila analyzed by breakage of ethological barriers. Genetics 147:231–242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  181. Sánchez‐Guillén, R. A. , Córdoba‐Aguilar A., Cordero‐Rivera A., and Wellenreuther M.. 2014. Genetic divergence predicts reproductive isolation in damselflies. J. Evol. Biol 27:76–87. [DOI] [PubMed] [Google Scholar]
  182. Sasa, M. M. , Chippindale P. T., and Johnson N. A.. 1998. Patterns of postzygotic isolation in frogs. Evolution 52:1811–1820. [DOI] [PubMed] [Google Scholar]
  183. Sawamura, K. 2000. Genetics of hybrid inviability and sterility in Drosophila: the Drosophila melanogaster–Drosophila simulans case. Plant Spec. Biol 15:237–247. [Google Scholar]
  184. Sawamura, K. , Maehara K., Keira Y., Ishikawa H. O., Sasamura T., Yamakawa T., and Matsuno K.. 2014. A Test of double interspecific introgression of nucleoporin genes inDrosophila . G3: Genes, Genomes, Genetics 4:2101–2106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  185. Sawamura, K. , Taira T., and Watanabe T. K.. 1993a. Hybrid lethal systems in the Drosophila melanogaster species complex. I. The maternal hybrid rescue (mhr) gene of Drosophila simulans . Genetics 133:299–305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  186. Sawamura, K. , and Yamamoto M. T.. 1993. Cytogenetical localization of Zygotic hybrid rescue (Zhr), a Drosophila melanogaster gene that rescues interspecific hybrids from embryonic lethality. MGG Molecular & General Genetics 239:441–449. [DOI] [PubMed] [Google Scholar]
  187. Sawamura, K. , Yamamoto M. T., and Watanabe T. K.. 1993b. Hybrid lethal systems in the Drosophila melanogaster species complex. II. The Zygotic hybrid rescue (Zhr) gene of D. melanogaster . Genetics 133:307–313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  188. Sawamura, K. , Davis A. W., and Wu C. I., 2000. Genetic analysis of speciation by means of introgression into Drosophila melanogaster . Proc. Natl. Acad. Sci. U. S. A 97:2652–2655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  189. Schaefer, H. M. , and Ruxton G. D.. 2015. Signal Diversity, Sexual Selection, and Speciation. Annu. Rev. Ecol. Evol. Syst 46:573–592. [Google Scholar]
  190. Schemske, D. W. 2010. Adaptation and the origin of species. Am. Nat 176:S4–S25. [DOI] [PubMed] [Google Scholar]
  191. Schemske, D. W. , Mittelbach G. G., Cornell H. V., Sobel J. M., and Roy K.. 2009. Is there a latitudinal gradient in the importance of biotic interactions? Annu. Rev. Ecol. Evol. Syst 40:245–269. [Google Scholar]
  192. Schilthuizen, M. , Giesbers M., and Beukeboom L. W.. 2011. Haldane's rule in the 21st century. Heredity 107:95–102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  193. Schlichting, C. D. , and Mousseau T. A.. 2009. The Year in Evolutionary Biology 2009, Volume 1168. [Google Scholar]
  194. Schumer, M. , Cui R., Rosenthal G. G., and Andolfatto P.. 2015. Reproductive isolation of hybrid populations driven by genetic incompatibilities. PLos Genet 11:e1005041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  195. Schumer, M. , Rosenthal G. G., and Andolfatto P.. 2014. How common is homoploid hybrid speciation? Evolution 68:1553–1560. [DOI] [PubMed] [Google Scholar]
  196. Schumer, M. , Rosenthal G. G., and Andolfatto P.. 2018. What do we mean when we talk about hybrid speciation? Heredity 120:379–382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  197. Scopece, G. , Musacchio A., Widmer A., and Cozzolino S.. 2007. Patterns of reproductive isolation in Mediterranean deceptive orchids. Evolution 61:2623–2642. [DOI] [PubMed] [Google Scholar]
  198. Scopece, G. , Widmer A., and Cozzolino S.. 2008. Evolution of postzygotic reproductive isolation in a guild of deceptive orchids. Am. Nat 171:315–326. [DOI] [PubMed] [Google Scholar]
  199. Scopece, G. , Musacchio A., Widmer A., and Cozzolino S., 2009. Contrasting thoughts about deceptive orchids: a response to Sobel and Randle. Evolution 63:2205–2209. [DOI] [PubMed] [Google Scholar]
  200. Seehausen, O. 2004. Hybridization and adaptive radiation. Trends Ecol. Evol 19:198–207. [DOI] [PubMed] [Google Scholar]
  201. Seehausen, O. , Butlin R. K., Keller I., Wagner C. E., Boughman J. W., Hohenlohe P. A., Peichel C. L., Saetre G. P., Bank C., Brännström A., et al. 2014. Genomics and the origin of species. Nat. Rev. Genet 15:176–192. [DOI] [PubMed] [Google Scholar]
  202. Serrato‐Capuchina, A. , Schwochert T. D., Zhang S., Roy B., Peede D., Koppelman C., and Matute D. R.. 2020. Pure species discriminate against hybrids in the Drosophila melanogaster species subgroup. bioRxiv 2020.07.22.214924. [DOI] [PubMed] [Google Scholar]
  203. Servedio, M. R. 2001. Beyond reinforcement: The evolution of premating isolation by direct selection on preferences and postmating, prezygotic incompatibilities. Evolution 55:1909–1920. [DOI] [PubMed] [Google Scholar]
  204. Servedio, M. R. 2011. Limits to the evolution of assortative mating by female choice under restricted gene flow. Proc. Roy. Soc. B 278:179–187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  205. Servedio, M. R. , and Kirkpatrick M.. 1997. The effects of gene flow on reinforcement. Evolution 51:1764–1772. [DOI] [PubMed] [Google Scholar]
  206. Servedio, M. R. , and Noor M. A. F.. 2003. The role of reinforcement in speciation: Theory and data. Annu. Rev. Ecol. Evol. Syst 34:339–364. [Google Scholar]
  207. Servedio, M. R. , and Saetre G.‐P.. 2003. Speciation as a positive feedback loop between postzygotic and prezygotic barriers to gene flow. Proc. R. Soc. B 270:1473–1479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  208. Shapiro, M. D. , Marks M. E., Peichel C. L., Blackman B. K., Nereng K. S., Jónsson B., Schluter D., and Kingsley D. M.. 2004. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428:717–723. [DOI] [PubMed] [Google Scholar]
  209. Singer, M. C. , and McBride C. S.. 2010. Multitrait, host‐associated divergence among sets of butterfly populations: implications for reproductive isolation and ecological speciation. Evolution: 64:921–933. [DOI] [PubMed] [Google Scholar]
  210. Singhal, S. , Huang H., Grundler M. R., Marchán‐Rivadeneira M. R., Holmes I., Title P. O., Donnellan S. C., and Rabosky D. L.. 2018. Does population structure predict the rate of speciation? A comparative test across Australia's most diverse vertebrate radiation. Am. Nat 192:432–447. [DOI] [PubMed] [Google Scholar]
  211. Sobel, J. M. , Chen G. F., Watt L. R., and Schemske D. W.. 2010. The biology of speciation. Evolution 64:295‐315. [DOI] [PubMed] [Google Scholar]
  212. Sobel, J. M. , and Randle A. M.. 2009. Comparative approaches to the evolution of reproductive isolation: A comment on Scopece Et Al. 2007. Evolution 63:2201–2204. [DOI] [PubMed] [Google Scholar]
  213. Sota, T. , and Tanabe T.. 2010. Multiple speciation events in an arthropod with divergent evolution in sexual morphology. Proc. R. Soc. B 277:689–696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  214. Spencer, H. G. , McArdle B. H., and Lambert D. M.. 1986. A theoretical investigation of speciation by reinforcement. Am. Nat 128:241–262. [Google Scholar]
  215. Stelkens, R. B. , Schmid C., Selz O., and Seehausen O., 2009. Phenotypic novelty in experimental hybrids is predicted by the genetic distance between species of cichlid fish. BMC Evol. Biol 9:283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  216. Stelkens, R. B. and Seehausen O.. 2009. Phenotypic divergence but not genetic distance predicts assortative mating among species of a cichlid fish radiation. Journal of Evolutionary Biology 22:1679–1694. [DOI] [PubMed] [Google Scholar]
  217. Templeton, A. R. 1981. Mechanisms of Speciation ‐ A population genetic approach. Annual Review of Ecology and Systematics 12:23–48. [Google Scholar]
  218. Throckmorton, L. H. 1982. Pathways of evolution in the genusDrosophila and the founding of the repleta group. Ecological genetics and evolution: the cactus‐yeast‐Drosophila model system edited Barker J. S. F., Starmer W. T.. Sydney; New York: Academic Press, 1982. [Google Scholar]
  219. Throckmorton, L. H. 1975. The phylogeny, ecology, and geography of Drosophila .
  220. Tiffin, P. , Olson S., and Moyle L. C.. 2001. Asymmetrical crossing barriers in angiosperms. Proc. R. Soc. B 268:861–867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  221. Tilley, S. G. , Verrell P. A., and Arnold S. J.. 1990. Correspondence between sexual isolation and allozyme differentiation: a test in the salamander Desmognathus ochrophaeus . Proc. Natl. Acad. Sci. U. S. A 87:2715–2719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  222. Traut, W. , Sahara K., and Marec F.. 2007. Sex chromosomes and sex determination in Lepidoptera. Sex Dev 1:332–346. [DOI] [PubMed] [Google Scholar]
  223. True, J. R. , Weir B. S., and Laurie C. C., 1996. A genome‐wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans Genetics  142:819–837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  224. Turelli, M. , Barton N. H., and Coyne J. A.. 2001. Theory and speciation. Trends Ecol. Evol 16:330–343. [DOI] [PubMed] [Google Scholar]
  225. Turelli, M. , and Begun D. J.. 1997. Haldane's Rule and X‐chromosome size in Drosophila . Genetics 147:1799–1815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  226. Turelli, M. , and Moyle L. C.. 2007. Asymmetric postmating isolation: Darwin's corollary to Haldane's Rule. Genetics 176:1059–1088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  227. Turelli, M. , Lipkowitz J. R., and Brandvain Y.. 2014. On the Coyne and Orr‐Igin of Species: Effects of intrinsic postzygotic isolation, ecological differentiation, X‐chromosome size, and sympatry on Drosophila speciation. Evolution 68:1176–1187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  228. Turissini, D. A. , Comeault A. A., Liu G., Lee Y. C. G., and Matute D. R.. 2017. The ability of Drosophila hybrids to locate food declines with parental divergence. Evolution 71:960–973. [DOI] [PubMed] [Google Scholar]
  229. Turissini, D. A. , Liu G., David J. R., and Matute D. R.. 2015. The evolution of reproductive isolation in theDrosophila yakuba complex of species. J. Evol. Biol 28:557–575. [DOI] [PubMed] [Google Scholar]
  230. Turissini, D. A. , McGirr J. A., Patel S. S., David J. R., and Matute D. R.. 2018. The rate of evolution of postmating‐prezygotic reproductive isolation in Drosophila . Mol. Biol. Evol 35:312–334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  231. Vienne, D. M. D. , Refrégier G., Hood M. E., Guigue A., Devier B., Vercken E., Smadja C., Deseille A., and Giraud T.. 2009. Hybrid sterility and inviability in the parasitic fungal species complex Microbotryum . J. Evol. Biol 22:683–698. [DOI] [PubMed] [Google Scholar]
  232. Vrana, P. B. , Fossella J. A., Matteson P., del Rio T., O'Neill M. J., and Tilghman S. M.. 2000. Genetic and epigenetic incompatibilities underlie hybrid dysgenesis in Peromyscus . Nat. Genet 25:120–124. [DOI] [PubMed] [Google Scholar]
  233. Wallace, A. R. 1865. On the phenomena of variation and geographical distribution as illustrated by the Papilionidae of the Malayan region. Transactions of the Linnean Society of London 25:1–71. [Google Scholar]
  234. Wallace, A. R. , 1889. Darwinism, an exponent of the theory of natural selection, with some of its applications. Macmillan and Company. [Google Scholar]
  235. Wang, R. J. , White M. A., and Payseur B. A.. 2015. The pace of hybrid incompatibility evolution in house mice. Genetics 201:229–242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  236. Weir, J. T. , and Wheatcroft D.. 2011. A latitudinal gradient in rates of evolution of avian syllable diversity and song length. Proc. R. Soc. B 278:1713–1720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  237. Widmer, A. , Lexer C., and Cozzolino S.. 2009. Evolution of reproductive isolation in plants. Heredity 102:31–38. [DOI] [PubMed] [Google Scholar]
  238. Wiens, J. J. , Engstrom T. N., and Chippindale P. T.. 2006. Rapid diversification, incomplete isolation, and the “speciation clock” in North American salamanders (genus Plethodon): Testing the hybrid swarm hypothesis of rapid radiation. Evolution 60:2585–2603. [PubMed] [Google Scholar]
  239. Wilkins, M. R. , Seddon N., and Safran R. J.. 2013. Evolutionary divergence in acoustic signals: causes and consequences. Trends Ecol. Evol 28:156–166. [DOI] [PubMed] [Google Scholar]
  240. Willig, M. R. , Kaufman D. M., and Stevens R. D.. 2003. Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis. Annual review of ecology. Evolution, and systematics 34:273–309. [Google Scholar]
  241. Williamson, D. L. and Ehrman L.. 1967. Induction of hybrid sterility in nonhybrid males of Drosophila paulistorum. Genetics 55:131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  242. Wilson, A. C. , Maxson L. R., and Sarich V. M.. 1974. Two types of molecular Evolution evidence from studies of interspecific hybridization. Proc. Natl. Acad. Sci. U. S. A 71:2843–2847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  243. Wu, C.‐I. 1992. A note on Haldane's Rule: hybrid inviability versus hybrid sterility. Evolution 46:1584–1587. [DOI] [PubMed] [Google Scholar]
  244. Wu, C.‐I. , Johnson N. A., and Palopoli M. F.. 1996. Haldane's rule and its legacy: Why are there so many sterile males? Trends Ecol. Evol 11:281–284. [DOI] [PubMed] [Google Scholar]
  245. Yamaguchi, R. , and Otto S. P.. 2020. Insights from Fisher's geometric model on the likelihood of speciation under different histories of environmental change. Evolution 74:1603–1619. [DOI] [PubMed] [Google Scholar]
  246. Yukilevich, R. 2012. Asymmetrical patterns of speciation uniquely support reinforcement in Drosophila . Evolution 66:1430–1446. [DOI] [PubMed] [Google Scholar]
  247. Yukilevich, R. 2013. Tropics accelerate the evolution of hybrid male sterility in Drosophila . Evolution 67:1805–1814. [DOI] [PubMed] [Google Scholar]
  248. Zouros, E. 1973. Genic differentiation associated with the early stages of speciation in the mulleri subgroup of Drosophila . Evolution 27:601–621. [DOI] [PubMed] [Google Scholar]

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