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. 2020 Oct 27;127(1):1–5. doi: 10.1093/aob/mcaa187

Propagule pressure and the establishment of emergent polyploid populations

Donald A Levin 1,
PMCID: PMC7750715  PMID: 33106838

Abstract

Background

Whereas the incidence or rate of polyploid speciation in flowering plants is modest, the production of polyploid individuals within local populations is widespread. Explanations for this disparity primarily have focused on properties or interactions of polyploids that limit their persistence.

Hypothesis

The emergence of local polyploid populations within diploid populations is similar to the arrival of invasive species at new, suitable sites, with the exception that polyploids suffer interference from their progenitor(s). The most consistent predictor of successful colonization by invasive plants is propagule pressure, i.e. the number of seeds introduced. Therefore, insufficient propagule pressure, i.e. the formation of polyploid seeds within diploid populations, ostensibly is a prime factor limiting the establishment of newly emergent polyploids within local populations. Increasing propagule number reduces the effects of genetic, environmental and demographic stochasticity, which thwart population survival. As with invasive species, insufficient seed production within polyploid populations limits seed export, and thus reduces the chance of polyploid expansion.

Conclusion

The extent to which propagule pressure limits the establishment of local polyploid populations remains to be determined, because we know so little. The numbers of auto- or allopolyploid seed in diploid populations rarely have been ascertained, as have the numbers of newly emergent polyploid plants within diploid populations. Moreover, seed production by these polyploids has yet to be assessed.

Keywords: Colonization, dispersal, invasion, polyploidy, population establishment, propagule pressure, seed production

INTRODUCTION

The frequency of polyploid speciation in flowering plants is low. It is estimated to be approximately between 15 % (Wood et al., 2009) and 24 % (Barker et al., 2016). Whereas speciation via ploidal shift has been quite infrequent, polyploid individuals have been generated in a multitude of plant species, with the propensity for and occurrence of polyploidization varying considerably among genotypes, populations and lineages (Husband et al., 2013). Given the considerable potential for a ploidal shift, it is surprising that the evolution of full-fledged species through ploidal increase has not occurred frequently. Why is this the case? It is generally accepted that the key obstacles to the establishment and spread of newly emergent polyploids are meiotic irregularities, and reduced fertility, altered gene dosage, instantly altered physiological properties, and minority cytotype disadvantage (Levin, 1975; Husband, 2000) and competitive inferiority (Baduel et al., 2018; Clark et al., 2019; Mandáková et al., 2019). Other obstacles may include few founding individuals or a paucity of genetic diversity in the founders (Hovick and Whitney, 2019) and reduced pollen fertility and fecundity (Levin, 2002; Huynh et al., 2020). Finally, polyploids may not perform well in their progenitor’s habitats (Maceira et al., 1993; McIntyre and Strauss, 2017; Hülber et al., 2018).

In contrast to properties or interactions of polyploids, I propose that insufficient production of polyploid seeds within local diploid populations constitutes an important, perhaps prime, factor limiting the establishment of persistent polyploid populations in suitable sites. To be sufficient the seed rain would have to be substantial within 1 year or the lifetime of the seeds. If diploid populations produced many polyploid seeds, but if they were well dispersed in time, the number of potential mates at any given time would be few, and the polyploid population would be below the minimum size for persistence.

The premise that insufficient polyploid seed production is a key factor in constraining polyploid establishment is based on the similarity between newly emergent polyploids within diploid populations and founders of new populations by invasive species. Like invasive colonists, these polyploids have the potential to establish local populations where they have never previously existed. Polyploid seeds are ‘imported’ from their local diploid progenitors, whereas seeds of an invasive plant population are imported from extraneous populations. Polyploids also are similar to invasive species in that their long-term persistence requires the availability of suitable sites and geographical expansion. Both polyploids and invasive species require a substantive number of seeds for successful local establishment at suitable sites. It should be noted that invasive species are preadapted to environments similar to those from which they emigrated, whereas polyploids may be less well adapted than resident diploids (Levin, 2002). If polyploids were maladapted, even copious seed production would not suffice for their establishment.

PROPAGULE PRESSURE IN INVASIVE SPECIES

The most consistent predictor of successful colonization by invasive plants is propagule pressure, the number of individuals introduced during a single colonization event (Williamson, 1996; Lockwood et al., 2005; Colautti et al., 2006; Simberloff, 2009; Blackburn et al., 2015). Increasing propagule number increases the probability of establishment principally by reducing the effects of genetic, environmental and demographic stochasticity (Fauvergue et al., 2012; Lande, 1988, 1993). Propagule pressure best predicts invasion success when establishment does not require significant evolutionary change (Peniston et al., 2019). The invasion of South Africa’s Agulhas Plain by woody species is better explained by propagule pressure than by specific environmental factors (Rouget and Richardson, 2003). The number of invaders introduced into riparian plots in southern California had a greater influence on invader numbers than did the richness of the resident species (Levine, 2000). Propagule pressure also is the fundamental driver of the invasion of Opuntia stricta in South Africa (Foxcroft et al., 2004) and Holcus lanatus into California (Thomsen et al., 2006). Most introductions to novel habitats by invasive plants fail in part because the immigration rate to suitable sites is too low (Lockwood et al., 2005; Zenni and Nuñez, 2013).

Cassey et al. (2018) evaluated the relationship between propagule pressure and establishment success for a broad range of taxa and life histories, including herbaceous plants and long-lived trees. They found a positive mean effect of propagule pressure on establishment success in every hypothesis tested and across experimental studies. Establishment probability is low for founding populations of ten or fewer individuals and highly likely as the number approaches 100. The strong effect of propagule number occurs in spite of location-level and species-level forces that can influence establishment success.

A continuing and substantive rain of seeds, particularly from a variety of sources, may enhance the likelihood of successful colonization because larger founder populations tend to contain more genetic and phenotypic diversity (Lande, 1988; Lockwood et al., 2005; Dlugosch and Parker, 2008; Fauvergue et al., 2012; Luque et al., 2016). Larger founder populations may contain increased genetic diversity, which may enhance colonization success. Increased diversity may increase rates of adaptation after introduction (Clegg and Allard, 1972; Reznick and Ghalambor, 2001) and reduce the level of inbreeding depression (Hufbauer et al., 2013). Increased diversity in self-incompatibility alleles will increase the number of potential mates. Even if genetic diversity is very low, small populations founded by high-performing colonists may still be successful due to their ability to self-fertilize (Siopa et al., 2020) or through the occurrence of genotypes whose critical population densities are low (de Groot et al., 2012; Sinclair et al., 2019).

Populations founded with the same number of individuals can vary substantially in their growth and persistence (Vahsen et al., 2018). Dependent variables are the extent of adaptedness to the new site (e.g. Hufbauer et al., 2012), how diverse founding groups are (e.g. Crawford and Whitney, 2010; Szucs et al., 2014), native range size (Schmidt et al., 2017) and the timing and frequency of discrete introduction events (e.g. Grevstad, 1999; Shea and Possingham, 2000). Establishment probability also is a function of the number of introductions. A continuing rain of seeds, particularly from a variety of sources, may enhance the likelihood of success (Simberloff, 2009). That a sparse seed rain is responsible for the failure of species recruitment into suitable sites has been demonstrated in seed addition and seed-trap studies in temperate (Turnbull et al., 2000; Foster and Tilman, 2003; Foster et al., 2004) and tropical communities (Dalling et al., 2002; Makana and Thomas, 2004; Svenning and Wright, 2005).

PROPAGULE PRESSURE IN POLYPLOIDS

Following the invasive species model, the number of seeds produced in a given diploid population ostensibly is a key factor in the initial establishment of a polyploid, as is the growth of the new population. The ‘invasion’ of a diploid population by a polyploid is not a single-season event. Rather, polyploids may be introduced as long as the diploid is present, which could be several years or only a few years in the case of weedy species. The polyploid seed rain is expected to vary in time, being a function of diploid population size and unreduced gamete production. There may be several pulses of high polyploid seed production, a few episodes, or none. A ‘drizzle’ of polyploid seeds is unlikely to yield a self-sustaining population, whereas pulses may. Unreduced gamete formation typically averages from 0.1 to 2.0 % in natural populations (Bretagnolle, 2001; Mason and Pires, 2015; Kreiner et al., 2017a, b). Different diploid populations would have different numerical dynamics and patterns of environmental stress, so that the propagule pressure certainly would vary among them in time and space. The greater the number of diploid populations and the larger their sizes, the higher is the probability that polyploid production would be sufficient for their establishment somewhere in the range of their diploid antecedents.

Unfortunately, our knowledge of the polyploid seed rain is extremely limited. No tetraploids were recovered in a sample of 6000 seeds in a diploid population of Anthoxanthum alpinum, but a few triploids were (three per thousand; Bretagnolle, 2001). The rate of hexaploid formation in the tetraploid Achillea borealis was 0.428 % (Ramsey, 2007). Hexaploid seeds have been produced in agricultural autotetraploid populations such as Beta vulgaris (2 %; Hornsey, 1973). Given a rate of 0.004 for the production of unreduced gametes, Ramsey and Schemske (1998) estimated that the rate of autotetraploid formation would be approximately two in 100 000. This estimate is of the same order (10−5) as those of the genic mutation rate obtained from studies in many organisms. These considerations indicate that a very large of number of seeds produced within a generation would be required for the establishment of polyploid populations. It follows that only very large diploid populations would host autopolyploid establishment. Large numbers of diploid hybrids would be required to produce the requisite number of allotetraploid seeds.

The production of allopolyploid seeds within diploid populations is a function of many variables, including the sizes of the two diploid species’ populations, as well as their phenological similarity and cross-compatibility, the viability of their hybrids, and the penchant of the latter to produce unreduced gametes. Allopolyploid production also would be correlated with the spatial proximity of the species and the frequency of hybridization. Given that two species hybridize frequently, allopolyploid seeds are more likely to be produced than autopolyploid seeds (Ramsey and Schemske, 1998). However, populations of most diploids do not have cross-compatible relatives growing within pollination range, so the incidence of hybridization must be very low, perhaps as low as 5 % (Marques et al., 2017).

Data on allopolyploid production are very sparse. From greenhouse studies, Grant (1952) estimated that the rate of polyploid production in hybrids of Gilia millefoliata and G. achilleaefolia was roughly 1.0 amphiploid per individual in 1949 and 0.18 amphiploids in 1951. The F1 hybrids between G. clokeyi and G. mexicana yielded 0.67 tetraploids per plant, and those between G. clokeyi and G. aliquanta yielded two tetraploids per plant (Grant, 2002). Marshall and Abbott (1980) estimated that the frequency of triploid hybrid formation between the diploid Senecio squalidus and the tetraploid S. vulgaris was 0.0126 %, based on 15 861 progeny tests. This triploid is the progenitor of the hexaploid S. cambrensis.

Given the production of polyploid seed, how many plants within a population are newly emergent polyploids? This question is most difficult to answer, in part because it usually is impossible to discern which polyploids are of immediate origins and which ones were produced in earlier years. Taking advantage of a difference in genome size between newly formed (neo)tetraploids and long-established tetraploids, Čertner et al. (2017) estimated the percentage of neotetraploids in numerous (1209) populations of Tripleurospermum inodorum that contained diploids and long-established tetraploids. Neotetraploids constituted only 0.03 % of all tetraploids; they occurred solitarily.

Once a diploid population contains some polyploid plants and the site remains hospitable, polyploid persistence depends on their seed production; this will be a function of plant number and vigour, competitive interactions and the breeding system. The more seeds produced, the higher the probability that polyploids will persist. Reproduction without the requirement for outcrossing will increase the level of seed production. Partial selfing increases the probability that newly founded populations persist because population sizes will increase faster and perhaps to a greater extent than with cross-breeding (Pannell et al., 2015). Self-fertility mitigates the minority cytotype mating disadvantage faced by rare polyploids (Levin, 1975).

Some polyploids have a penchant for asexual reproduction, which may increase the potential for population establishment and persistence in times of low seed production (Hörandl, 2006; Robertson et al., 2010; Kolář et al., 2017; Van Drunen and Husband, 2019). Chromosome doubling may enhance the level of asexual reproduction already present in a progenitor. Consider the tetraploid Sorghum halepense (2n = 40), which arose through hybridization between S. bicolor (2n = 20), an annual, and the perennial S. propinquum (2n = 20). Rhizomes of S. halepense are more extensive than those of its rhizomatous progenitor S. propinquum (Paterson et al., 2020). The extent to which asexual reproduction facilitates the establishment of newly formed polyploids in local populations remains to be determined.

CONCLUSIONS

It is important to understand the factors influencing the establishment of polyploids in local diploid populations, because this process is a prime step in the evolution of a new species. Invasive species provide valuable insights into factors most important in polyploid establishment (Levin, 2019). Studies of invasive species indicate that the establishment of newly emergent polyploids initially is very likely contingent upon an adequate seed rain from diploids and the availability of suitable sites. The potential superiority of polyploids is irrelevant in this process; if they do not establish a persistent foothold and export seeds to suitable sites the lineage will most likely disappear.

Unfortunately, there is a dearth of knowledge about the importance of propagule pressure, which is pivotal in polyploid establishment. Hovick and Whitney (2019) investigated the relationship between propagule pressure and the likelihood of population persistence in a seed addition experiment using Arabidopsis thaliana. They demonstrated that the positive effect of propagule pressure lasted for only three generations, and subsequently was dependent on numerous factors. There is no corresponding information on strictly outcrossing species, whose initial populations may experience Allee effects and inbreeding depression (Kramer et al., 2009; Szucs et al., 2014).

There is a huge disparity between what we know about invasives and polyploids. We know very little about polyploid seed production by diploid plants, and the number of polyploid plants arising from such. If the successful transitions from diploidy to polyploidy were based in part on propagule pressure, then we should study species in which this transition has occurred multiple times. Consider first an example involving autotetraploids. Galax urceolata, which is a herbaceous, self-incompatible perennial, has arisen independently at least 46 times (Servick et al., 2015). This is among the highest frequencies of independent polyploidizations known for an auto- or allopolyploid. There are numerous questions that can be asked about this species relative to the thesis of the paper. How many tetraploid seeds are produced by diploid plants, and to what extent does it vary among plants and populations? How many tetraploid plants occur within diploid populations? How many seeds do tetraploid plants produce, and to what extent does the number vary among plants and populations?

Populations containing pairs of Tragopogon species (T. dubius, T. pratensis, T. porrifolius) and their tetraploid derivatives (T. mirus derived from P. porrifolius and T. dubius; T. miscellus derived from T. pratensis and T. dubius) would be excellent venues for assessing the early ingredients of allotetraploid success. The tetraploids are the products of multiple independent origins within the past century (Soltis et al., 2004). The diploid species occur jointly at some locations, as do tetraploids and their progenitors. Both allotetraploids form numerous populations, some with thousands of plants (Novak et al., 1991). Some of the questions that could be asked of this system are as follows. How many seeds of each parental species are F1 hybrids? How many tetraploid seeds do the hybrids produce? How many hybrids are present in natural populations? How many tetraploids are present in natural populations? How many seeds do tetraploid plants produce? Empirical estimates (available and to be obtained) should shed light on the paradoxical paucity of neopolyploids in natural populations and on the regularity of multiple origins as judged from molecular surveys.

ACKNOWLEDGEMENTS

The author is most grateful to Trude Schwarzacher and two anonymous reviewers for their thoughtful critiques of the manuscript.

LITERATURE CITED

  1. Baduel P, Bray S, Vallejo-Marin M, Kolar F, Yant L. 2018. The “Polyploid Hop”: shifting challenges and opportunities over the evolutionary lifespan of genome duplications. Frontiers in Ecology and Evolution 6: 1–19. [Google Scholar]
  2. Barker MS, Arrigo N, Baniaga AE, Li Z, Levin DA. 2016. On the relative abundance of autopolyploids and allopolyploids. New Phytologist 210: 391–398. [DOI] [PubMed] [Google Scholar]
  3. Blackburn TM, Lockwood JL, Cassey P. 2015. The influence of numbers on invasion success. Molecular Ecology 24: 1942–1953. [DOI] [PubMed] [Google Scholar]
  4. Bretagnolle F 2001. Pollen production and spontaneous polyploidization in diploid populations of Anthoxanthum alpinum. Biological Journal of the Linnean Society 72: 241–247. [Google Scholar]
  5. Cassey P, Delean S, Lockwood JL, Sadowski JS, Blackburn TM. 2018. Dissecting the null model for biological invasions: a meta-analysis of the propagule pressure effect. PLoS Biology 16: e2005987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Čertner M, Fenclová E, Kúr P, et al. 2017. Evolutionary dynamics of mixed-ploidy populations in an annual herb: dispersal, local persistence and recurrent origins of polyploids. Annals of Botany 120: 303–315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Clark LV, Jin X, Petersen KK, et al. 2019. Population structure of Miscanthus sacchariflorus reveals two major polyploidization events, tetraploid-mediated unidirectional introgression from diploid M. sinensis, and diversity centred around the Yellow Sea. Annals of Botany 124: 731–748. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Clegg MT, Allard RW. 1972. Patterns of genetic differentiation in the slender wild oat species Avena barbata. Proceedings of the National Academy of Sciences of the USA 69: 1820–1824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Colautti RI, Grigorovich IA, MacIsaac HJ. 2006. Propagule pressure: a null model for biological invasions. Biological Invasions 8: 1023–1037. [Google Scholar]
  10. Crawford KM, Whitney KD. 2010. Population genetic diversity influences colonization success. Molecular Ecology 19: 1253–1263. [DOI] [PubMed] [Google Scholar]
  11. Dalling JW, Muller-Landau HC, Wright SJ, Hubbell SP. 2002. Role of dispersal in recruitment limitation of neotropical pioneer species. Journal of Ecology 90: 714–727 [Google Scholar]
  12. Dlugosch KM, Parker IM. 2008. Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology 17: 431–449. [DOI] [PubMed] [Google Scholar]
  13. Van Drunen WE, Husband BC. 2019. Evolutionary associations between polyploidy, clonal reproduction, and perenniality in the angiosperms. New Phytologist 224: 1266–1277. [DOI] [PubMed] [Google Scholar]
  14. Fauvergue X, Vercken E, Malausa T, Hufbauer RA. 2012. The biology of small, introduced populations, with special reference to biological control. Evolutionary Applications 5: 424–443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Foster BL, Tilman D. 2003. Seed limitation and regulation of community structure on oak savanna grassland. Journal of Ecology 91: 999–1007. [Google Scholar]
  16. Foster BL, Dickson TL, Murphy CA, Karel IS, Smith VH. 2004. Propagule pools mediate community assembly and ecosystem-diversity regulation along a grassland productivity gradient. Journal of Ecology 92: 435–444. [Google Scholar]
  17. Foxcroft LC, Rouget M, Richardson DM, MacFadyen S. 2004. Reconstructing 50 years of Opuntia stricta invasion in the Kruger National Park, South Africa: environmental determinants and propagule pressure. Diversity and Distributions 10: 427–37. [Google Scholar]
  18. Grant V 1952. Cytogenetics of the hybrid Gilia millefoliata × achilleaefolia. I. Variations in meiosis and polyploidy rate as affected by nutritional and genetic conditions. Chromosoma 5: 372–390. [PubMed] [Google Scholar]
  19. Grant V 2002. Frequency of spontaneous amphiploids in Gilia (Polemoniaceae) hybrids. American Journal of Botany 89: 1197–1202. [DOI] [PubMed] [Google Scholar]
  20. Grevstad FS 1999. Factors influencing the chance of population establishment: implications for release strategies in biological control. Ecological Applications 9: 1439–1447. [Google Scholar]
  21. de Groot GA, Verduyn B, Wubs ER, Erkens RH, During HJ. 2012. Inter- and intraspecific variation in fern mating systems after long-distance colonization: the importance of selfing. BMC Plant Biology 12: 3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hörandl E 2006. The complex causality of geographical parthenogenesis. New Phytologist 171: 525–538. [DOI] [PubMed] [Google Scholar]
  23. Hornsey KG 1973. The occurrence of hexaploid plants among autotetraploid populations of sugar beet (Beta vulgaris L.), and the production of tetraploid progeny using a diploid pollinator. Caryologia 26: 225–228. [Google Scholar]
  24. Hovick SM, Whitney KD. 2019. Propagule pressure and genetic diversity enhance colonization by a ruderal species: a multi-generation field experiment. Ecological Monographs 8: e01368. [Google Scholar]
  25. Hufbauer RA, Facon B, Ravigné V, et al. 2012. Anthropogenically induced adaptation to invade (AIAI): contemporary adaptation to human-altered habitats within the native range can promote invasions. Evolutionary Applications 5: 89–101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hufbauer RA, Rutschmann A, Serrate B, Vermeil de Conchard H, Facon B. 2013. Role of propagule pressure in colonization success: disentangling the relative importance of demographic, genetic and habitat effects. Journal of Evolutionary Biology 26: 1691–1699. [DOI] [PubMed] [Google Scholar]
  27. Hülber K, Sonnleitner M, Haider J, et al. 2018. Reciprocal transplantations reveal strong niche differentiation among ploidy-differentiated species of the Senecio carniolicus aggregate (Asteraceae) in the easternmost Alps. Alpine Botany 128: 107–119. [Google Scholar]
  28. Husband BC 2000. Constraints on polyploid evolution: a test of the minority cytotype exclusion principle. Proceedings. Biological Sciences 267: 217–223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Husband BC, Baldwin SJ, Suda J. 2013. The incidence of polyploidy in natural plant populations: major patterns and evolutionary processes. In: Greilhuber J, Doleze J, Wendel JF, eds. Plant genome diversity, Vol. 2 Vienna: Springer, 255–276. [Google Scholar]
  30. Huynh S, Broennimann O, Guisan A, Felber F, Parisod C. 2020. Eco-genetic additivity of diploids in allopolyploid wild wheats. Ecology Letters 23: 663–673. [DOI] [PubMed] [Google Scholar]
  31. Kolář F, Čertner M, Suda J, Schönswetter P, Husband B. 2017. Mixed-ploidy species: progress and opportunities in polyploid research. Trends in Plant Science 22: 1041–1055. [DOI] [PubMed] [Google Scholar]
  32. Kramer AM, Dennis B, Liebhold AM, Drake JA. 2009. The evidence for Allee effects. Population Ecology 51: 341–354. [Google Scholar]
  33. Kreiner JM, Kron P, Husband BC. 2017a Frequency and maintenance of unreduced gametes in natural plant populations: associations with reproductive mode, life history and genome size. New Phytologist 214: 879–889. [DOI] [PubMed] [Google Scholar]
  34. Kreiner JM, Kron P, Husband BC. 2017b evolutionary dynamics of unreduced gametes. Trends in Genetics 33: 583–593. [DOI] [PubMed] [Google Scholar]
  35. Lande R 1988. Genetics and demography in biological conservation. Science 241: 1455–1460. [DOI] [PubMed] [Google Scholar]
  36. Lande R 1993. Risks of population extinction from demographic and environmental stochasticity and random catastrophes. American Naturalist 142: 911–927. [DOI] [PubMed] [Google Scholar]
  37. Levin DA 1975. Minority cytotype exclusion in local plant populations. Taxon 24: 35–43. [Google Scholar]
  38. Levin DA 2019. Plant speciation in the age of climate change. Annals of Botany 124: 769–775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Levin DA 2002. The role of chromosomal change in plant evolution. New York: Oxford University Press. [Google Scholar]
  40. Levine JM 2000. Species diversity and biological invasions: relating local process to community pattern. Science 288: 852–54. [DOI] [PubMed] [Google Scholar]
  41. Lockwood JL, Cassey P, Blackburn T. 2005. The role of propagule pressure in explaining species invasions. Trends in Ecology & Evolution 20: 223–228. [DOI] [PubMed] [Google Scholar]
  42. Luque GM, Vayssade C, Facon B, Guillemaud T, Courchamp F, Fauvergue X. 2016. The genetic Allee effect: a unified framework for the genetics and demography of small populations. Ecosphere 7: e01413. [Google Scholar]
  43. Maceira NO, Jacquard P, Lumerat R. 1993. Competition between diploid and derivative autotetraploid Dactylis glomerata L. from Galicia. Implications for the establishment of novel polyploid populations. New Phytologist 124: 321–328. [DOI] [PubMed] [Google Scholar]
  44. Makana JR, Thomas C. 2004. Dispersal limits recruitment of African mahoganies. Oikos 106: 67–72. [Google Scholar]
  45. Mandáková T, Zozomová-Lihová J, Kudoh H, Zhao Y, Lysak MA, Marhold K. 2019. The story of promiscuous crucifers: origin and genome evolution of an invasive species, Cardamine occulta (Brassicaceae), and its relatives. Annals of Botany 124: 209–220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Marques I, Loureiro J, Draper D, Castro M, Castro S. 2017. How much do we know about the frequency of hybridization and polyploidy in the Mediterranean region? Plant Biology 20 (Suppl. 1): 21–37. [DOI] [PubMed] [Google Scholar]
  47. Marshall DF, Abbott RJ. 1980. On the frequency of introgression of the radiate (Tr) allele from Senecio squalidus L. into Senecio vulgaris L. Heredity 45: 133–135. [Google Scholar]
  48. Mason AS, Pires JC. 2015. Unreduced gametes: meiotic mishap or evolutionary mechanism? Trends in Genetics 31: 5–10. [DOI] [PubMed] [Google Scholar]
  49. McIntyre PJ, Strauss S. 2017. An experimental test of local adaptation among cytotypes within a polyploid complex. Evolution 71: 1960–1969. [DOI] [PubMed] [Google Scholar]
  50. Novak SJ, Soltis DE, Soltis PS. 1991. Ownbey’s tragopogons: 40 years later. American Journal of Botany 78: 1586–1600. [Google Scholar]
  51. Pannell JR, Auld JR, Brandvain Y, et al. 2015. The scope of Baker’s law. New Phytologist 208: 656–667. [DOI] [PubMed] [Google Scholar]
  52. Paterson AH, Kong W, Johnston RM, et al. 2020. The evolution of an invasive plant, Sorghum halepense L. (‘Johnsongrass’). Frontiers in Genetics 11: 317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Peniston JH, Barfield M, Holt RD. 2019. Pulsed immigration events can facilitate adaptation to harsh sink environments. American Naturalist 194: 316–333. [DOI] [PubMed] [Google Scholar]
  54. Ramsey J 2007. Unreduced gametes and neopolyploids in natural populations of Achillea borealis (Asteraceae). Heredity 98: 143–150. [DOI] [PubMed] [Google Scholar]
  55. Ramsey J, Schemske DW. 1998. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annual Review of Ecology and Systematics 29: 467–501. [Google Scholar]
  56. Reznick DN, Ghalambor CK. 2001. The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112–113: 183–198. [PubMed] [Google Scholar]
  57. Robertson A, Rich TC, Allen AM, et al. 2010. Hybridization and polyploidy as drivers of continuing evolution and speciation in Sorbus. Molecular Ecology 19: 1675–1690. [DOI] [PubMed] [Google Scholar]
  58. Rouget M, Richardson DM. 2003. Inferring process from pattern in plant invasions: a semi-mechanistic model incorporating propagule pressure and environmental factors. American Naturalist 162: 713–724. [DOI] [PubMed] [Google Scholar]
  59. Schmidt JP, Drake JM, Stephens P. 2017. Residence time, native range size, and genome size predict naturalization among angiosperms introduced to Australia. Ecology and Evolution 7: 10289–10300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Servick S, Visger CJ, Gitzendanner MA, Soltis PS, Soltis DE. 2015. Population genetic variation, geographic structure, and multiple origins of autopolyploidy in Galax urceolata. American Journal of Botany 102: 973–982. [DOI] [PubMed] [Google Scholar]
  61. Shea K, Possingham HP. 2000. Optimal release strategies for biological control agents: an application of stochastic dynamic programming to population management. Journal of Applied Ecology 37: 77–86. [Google Scholar]
  62. Simberloff D 2009. The role of propagule pressure in biological invasions. Annual Review of Ecology, Evolution, and Systematics 40: 81–102. [Google Scholar]
  63. Sinclair JS, Arnott SE, Millette KL, Cristescu ME. 2019. Benefits of increased colonist quantity and genetic diversity for colonization depend on colonist identity. Oikos 128: 1761–1771. [Google Scholar]
  64. Siopa C, Dias MC, Castro M, Loureiro J, Castro S. 2020. Is selfing a reproductive assurance promoting polyploid establishment? Reduced fitness, leaky self-incompatibility and lower inbreeding depression in neotetraploids. American Journal of Botany 107: 526–538. [DOI] [PubMed] [Google Scholar]
  65. Soltis DE, Soltis PS, Pires JC, Kovarik A, Tate JA, Mavrodiev E. 2004. Recent and recurrent polyploidy in Tragopogon (Asteraceae): cytogenetic, genomic and genetic comparisons. Biological Journal of the Linnean Society 82: 485–501. [Google Scholar]
  66. Svenning J-C, Wright J. 2005. Seed limitation in a Panamanian forest. Journal of Ecology 93: 853–862. [Google Scholar]
  67. Szucs M, Melbourne BA, Tuff T, Hufbauer RA. 2014. The roles of demography and genetics in the early stages of colonization. Proceedings of the Royal Society, Series B. 281: 20141073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Thomsen MA, D’Antonio CM, Suttle KB, Sousa WP. 2006. Ecological resistance, seed density and their interactions determine patterns of invasion in a California coastal grassland. Ecology Letters 9: 160–170. [DOI] [PubMed] [Google Scholar]
  69. Turnbull LA, Crawley MJ, Rees M. 2000. Are plant populations seed-limited? A review of seed sowing experiments. Oikos 88: 225–238 [Google Scholar]
  70. Vahsen ML, Shea K, Hovis CL, Teller BJ, Hufbauer RA. 2018. Prior adaptation, diversity, and introduction frequency mediate the positive relationship between propagule pressure and the initial success of founding populations. Biological Invasions 20: 2451–2459. [Google Scholar]
  71. Williamson M 1996. Biological invasions. London: Chapman & Hall. [Google Scholar]
  72. Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH. 2009. The frequency of polyploid speciation in vascular plants. Proceedings of the National Academy of Sciences of the USA 106: 13875–13879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Zenni RD, Nuñez MA. 2013. The elephant in the room: the role of failed invasions in understanding invasion biology. Oikos 122: 801–815. [Google Scholar]

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