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Hybrid zones allow the measurement of gene flow across the genome, producing insight into the genomic architecture of speciation. Such analysis is particularly powerful when applied to multiple pairs of hybridizing species, as patterns of genomic differentiation can then be related to age of the hybridizing species, providing a view into the buildup of differentiation over time. We examined 33,809 single nucleotide polymorphisms (SNPs) in three hybridizing woodpecker species: Red-breasted, Red-naped, and Yellow-bellied sapsuckers (Sphyrapicus ruber, S. nuchalis, and S. varius), two of which (ruber and nuchalis) are much more closely related than each is to the third (varius). To identify positions of SNPs on chromosomes, we developed a localization method based on comparative genomics. We found narrow clines, bimodal distributions of hybrid indices, and genomic regions with decreased rates of introgression. These results suggest moderately strong reproductive isolation among species and selection against specific hybrid genotypes. We found 19 small regions of strong differentiation between species, partly shared among species pairs, but no large regions of differentiation. An association analysis revealed a single strong-effect candidate locus associated with plumage, possibly explaining mismatch among the three species in genomic relatedness and plumage similarity. Our comparative analysis of species pairs of different age and their hybrid zones showed that moderately strong reproductive isolation can occur with little genomic differentiation, but that reproductive isolation is incomplete even with much greater genomic differentiation, implying there are long periods of time when hybridization is possible if diverging populations are in geographic contact. This article is protected by copyright. All rights reserved.
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... nuchalis and S. ruber/S. varius hybrid zones have been studied both behaviourally and genetically (Johnson and Zink 1983, Johnson and Johnson 1985, Cicero and Johnson 1995, Seneviratne et al. 2012, 2016, 2019, Grossen et al. 2016, Natola and Burg 2018. Though these species hybridize, studies of mate choice in two hybrid zones show the forms mate assortatively, supporting their designations as separate species (Johnson and Johnson 1985, Seneviratne et al. 2012, 2016. ...
... We note that they are the two forms that look most alike, though they are not each other's closest relatives Zink 1983, Cicero andJohnson 1995). Indeed, hybridization between the two species does not appear to be prevented by their strong genetic differentiation -F ST between S. nuchalis and S. varius (0.26 this study, 0.23 Grossen et al. 2016) is large compared to either species and S. ruber (0.18 ruber/varius, 0.06 ruber/nuchalis, Grossen et al. 2016). This raises an intriguing question: how can assortative mating limit introgression if mate choice is based on a trait that is not closely associated with ancestry, a phenomenon recently described by Semenov et al. (2017) in white wagtails Motacilla alba. ...
... We note that they are the two forms that look most alike, though they are not each other's closest relatives Zink 1983, Cicero andJohnson 1995). Indeed, hybridization between the two species does not appear to be prevented by their strong genetic differentiation -F ST between S. nuchalis and S. varius (0.26 this study, 0.23 Grossen et al. 2016) is large compared to either species and S. ruber (0.18 ruber/varius, 0.06 ruber/nuchalis, Grossen et al. 2016). This raises an intriguing question: how can assortative mating limit introgression if mate choice is based on a trait that is not closely associated with ancestry, a phenomenon recently described by Semenov et al. (2017) in white wagtails Motacilla alba. ...
Article
Studying species interactions at hybrid zones allows biologists to understand the forces that promote speciation. Hybridization among Sphyrapicus nuchalis, S. varius and S. ruber has long been acknowledged, and hybrid zones between S. nuchalis/S. ruber and S. varius/S. ruber have been characterized with both genetic and genomic data. Using a combination of next‐generation restriction site‐associated DNA sequencing (RAD‐Seq) and traditional genetic methods, we examined patterns of introgression in the poorly characterized S. nuchalis/S. varius contact zone; the two most similar species in the complex, though they are not each other's closest relatives. We found high introgression rates, with several early and many advanced generation hybrids along a 275 km stretch of Rocky Mountain foothill, pointing to a well‐established hybrid zone with hybrid individuals backcrossing with individuals from the parental species and each other. Plumage colouration in the hybrid zone was a relatively poor indicator of parental or hybrid status, which could be attributed to the possible involvement of few large effect genes.
... While speciation is often defined as the evolution of reproductive isolation (Mayr 1942;Coyne and Orr 2004), recent empirical and theoretical work has demonstrated that distinct species can persist in the presence of gene flow. This phenomenon may occur by sympatric divergence with gene flow (primary gene flow; Niemiller et al. 2008;Martin et al. 2013), or more commonly is the result of allopatric speciation followed by secondary contact (secondary gene flow; Tarroso et al. 2014;Grossen et al. 2016). Many species are maintained in nature despite some level of gene exchange, either coexisting in sympatry due to niche and/or phenotypic divergence (e.g., Whittemore and Schaal 1991;Milne et al. 1999;Neaves et al. 2010;Hochkirch and Lemke 2011); or replacing each other abruptly at narrow contact zones (e.g., Szymura and Barton 1986;Irwin et al. 2009;Tarroso et al. 2014;Grossen et al. 2016). ...
... This phenomenon may occur by sympatric divergence with gene flow (primary gene flow; Niemiller et al. 2008;Martin et al. 2013), or more commonly is the result of allopatric speciation followed by secondary contact (secondary gene flow; Tarroso et al. 2014;Grossen et al. 2016). Many species are maintained in nature despite some level of gene exchange, either coexisting in sympatry due to niche and/or phenotypic divergence (e.g., Whittemore and Schaal 1991;Milne et al. 1999;Neaves et al. 2010;Hochkirch and Lemke 2011); or replacing each other abruptly at narrow contact zones (e.g., Szymura and Barton 1986;Irwin et al. 2009;Tarroso et al. 2014;Grossen et al. 2016). Thus, it has been increasingly accepted that speciation can occur without complete reproductive isolation (Mallet 2008;Pinho and Hey 2010) and complete reproductive isolation is not a pre-requisite for most current species definitions such as the Evolutionary Species Concept (Simpson 1961) or even for most current versions of the Biological Species Concept originally proposed by Mayr (1940Mayr ( , 1942. ...
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Recent empirical studies have demonstrated that speciation with gene flow is more common than previously thought. From a conservation perspective, the potential negative effects of hybridization raise concerns on the genetic integrity of endangered species. However, introgressive hybridization has also been growingly recognized as a source of diversity and new advantageous alleles. Carbonell's wall lizard (Podarcis carbonelli) is an endangered species whose distribution overlaps with four other congeneric species. Our goal here was to determine whether P. carbonelli is completely reproductively isolated from its congeners and to evaluate the relevance of hybridization and interspecific gene flow for developing a conservation plan. We used restriction site associated DNA (RAD) sequencing to discover SNPs in samples from four contact zones between P. carbonelli and four other species. Principal component analysis, multilocus genotype assignment and interspecific heterozygosity suggest incomplete reproductive isolation and ongoing gene flow between species. However, hybridization dynamics vary across all pairs, suggesting complex interactions between multiple intrinsic and extrinsic barriers. Despite seemingly ubiquitous interspecific gene flow, we found evidence of strong reproductive isolation across most contact zones. Instead, indirect effects of hybridization like waste of reproductive effort in small isolated populations may be more problematic. Our results highlight the need to further evaluate the consequences of introgression for P. carbonelli, both on a geographic and genomic level and included in a comprehensive and urgently needed conservation plan. Besides, those findings will add important insights on the potential effects of hybridization and introgression for endangered species.
... Additionally, phylogenomic analyses routinely detect population admixture and hybridization, which can both generate and reduce biodiversity (e.g., Lamichhaney et al., 2015;Grossen et al., 2016;Kearns et al., 2018;Lavretsky et al., 2019). Introgression can be a frequent source of cytonuclear discordance via plastid capture (e.g., Hawkins et al., 2016), necessitating the analysis of both nuclear and plastid sequences to reconstruct the species tree. ...
... For these loci, the excess of S. senegalensis ancestry 456 (measured by the genomic cline parameter α) was positively related to the extent of the spatial 457 shift of the cline center into the S. aegyptiaca territory. This correlation was much stronger 458 than previously observed in a bird hybrid zone study(Grossen et al., 2016), possibly due to a 459 stronger variance in cline shift in the Solea system. By contrast, much fewer loci were found460 with increased introgression rates in the opposite direction. ...
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Investigating variation in gene flow across the genome between closely related species is important to understand how reproductive isolation builds up during the speciation process. An efficient way to characterize differential gene flow is to study how the genetic interactions that take place in hybrid zones selectively filter gene exchange between species, leading to heterogeneous genome divergence. In the present study, genome-wide divergence and introgression patterns were investigated between two sole species, Solea senegalensis and Solea aegyptiaca , using a restriction-associated DNA sequencing (RAD-Seq) approach to analyze samples taken from a transect spanning the hybrid zone. An integrative approach combining geographic and genomic clines methods with an analysis of individual locus introgression taking into account the demographic history of divergence inferred from the joint allele frequency spectrum was conducted. Our results showed that only a minor fraction of the genome can still substantially introgress between the two species due to genome-wide congealing. We found multiple evidence for a preferential direction of introgression in the S. aegyptiaca genetic background, indicating a possible recent or ongoing movement of the hybrid zone. Deviant introgression signals found in the opposite direction supported that the Mediterranean populations of S. senegalensis could have benefited from adaptive introgression. Our study thus illustrates the varied outcomes of genetic interactions between divergent gene pools that recently met after a long history of divergence.
... In line with the ADMIXTURE-analyses, the genetic divergence between the taxa seems to be driven by few genomic regions that are scattered throughout the genome, so-called islands of differentiation (Figs. 2 and 3). This pattern has been observed in other bird species, such as crows (Poelstra et al. 2014), woodpeckers (Grossen et al. 2016), warblers (Toews et al. 2016;Irwin et al. 2018), flycatchers (Ellegren et al. 2012;Burri et al. 2015), thrushes (Ruegg et al. 2014;Delmore et al. 2015), stonechats (Van Doren et al. 2017), and nightingales (Mořkovský et al. 2018). In line with previous studies, we found no significant difference in the level of genetic differentiation between islands on autosomes and on the Z-chromosome (e.g., Ellegren et al. 2012;Bay and Ruegg 2017;Mořkovský et al. 2018). ...
Article
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Several studies have uncovered a highly heterogeneous landscape of genetic differentiation across the genomes of closely related species. Specifically, genetic differentiation is often concentrated in particular genomic regions (“islands of differentiation”) that might contain barrier loci contributing to reproductive isolation, whereas the rest of the genome is homogenized by introgression. Alternatively, linked selection can produce differentiation islands in allopatry without introgression. We explored the influence of introgression on the landscape of genetic differentiation in two hybridizing goose taxa: the Taiga Bean Goose (Anser fabalis) and the Tundra Bean Goose (A. serrirostris). We re-sequenced the whole genomes of 18 individuals (9 of each taxon) and, using a combination of population genomic summary statistics and demographic modeling, we reconstructed the evolutionary history of these birds. Next, we quantified the impact of introgression on the build-up and maintenance of genetic differentiation. We found evidence for a scenario of allopatric divergence (about 2.5 million years ago) followed by recent secondary contact (about 60,000 years ago). Subsequent introgression events led to high levels of gene flow, mainly from the Tundra Bean Goose into the Taiga Bean Goose. This scenario resulted in a largely undifferentiated genomic landscape (genome-wide FST = 0.033) with a few notable differentiation peaks that were scattered across chromosomes. The summary statistics indicated that some peaks might contain barrier loci while others arose in allopatry through linked selection. Finally, based on the low genetic differentiation, considerable morphological variation and incomplete reproductive isolation, we argue that the Taiga and the Tundra Bean Goose should be treated as subspecies.
... Despite the widespread use of cline theory to infer selection in hybrid zones (e.g., Moore and Buchanan 1985;Hewitt 1988;Mallet et al. 1990;Alexandrino et al. 2005;Gay et al. 2008;Brelsford and Irwin 2009;Grossen et al. 2016), it requires a number of assumptions that may be questionable in specific empirical systems. One of these is the assumption of random mating at each location along the cline, which is ironic given the widespread opinion (see above) that prezygotic isolation is so important in the early stages of speciation. ...
Article
Partial prezygotic isolation is often viewed as more important than partial postzygotic isolation (low fitness of hybrids) early in the process of speciation. I simulate secondary contact between two populations (species) to examine effects of assortative mating and low hybrid fitness in preventing blending. A small reduction in hybrid fitness (e.g., by 10%) produces a narrower hybrid zone than a strong but imperfect mating preference (e.g., 10 times stronger preference for conspecific over heterospecific mates). In the latter case, rare F1 hybrids find each other attractive (due to assortative mating), leading to the buildup of a continuum of intermediates. The weakness of assortative mating compared with reduced fitness of hybrids in preventing blending is robust to varying genetic bases of these traits. Assortative mating is most powerful in limiting blending when it is encoded by a single locus or is essentially complete, or when there is a large mate search cost. In these cases assortative mating is likely to cause hybrids to have low fitness, due to frequency-dependent mating disadvantage of individuals of rare mating types. These results prompt a questioning of the concept of partial prezygotic isolation, since it is not very isolating unless there is also postzygotic isolation.
... However, the location of the genomic islands was specific to each hybrid zone (Vijay et al. 2016). A similar study on three hybridizing woodpecker species-Red-breasted (Sphyrapicus ruber), Red-naped (S. nuchalis) and Yellowbellied Sapsucker (S. varius)-reported a candidate locus for plumage colour that might be involved in reproductive isolation (Grossen et al. 2016). Contrary to the crow system, however, this locus was not located within a genomic island of differentiation. ...
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p>Hybridization is not always limited to two species; often multiple species are interbreeding. In birds, there are numerous examples of species that hybridize with multiple other species. The advent of genomic data provides the opportunity to investigate the ecological and evolutionary consequences of multispecies hybridization. The interactions between several hybridizing species can be depicted as a network in which the interacting species are connected by edges. Such hybrid networks can be used to identify 'hub-species' that interbreed with multiple other species. Avian examples of such 'hub-species' are Common Pheasant (Phasianus colchicus), Mallard (Anas platyrhynchos) and European Herring Gull (Larus argentatus). These networks might lead to the formulation of hypotheses, such as which connections are most likely conducive to interspecific gene flow (i.e. introgression). Hybridization does not necessarily result in introgression. Numerous statistical tests are available to infer interspecific gene flow from genetic data and the majority of these tests can be applied in a multispecies setting. Specifically, model-based approaches and phylogenetic networks are promising in the detection and characterization of multispecies introgression. It remains to be determined how common multispecies introgression in birds is and how often this process fuels adaptive changes. Moreover, the impact of multispecies hybridization on the build-up of reproductive isolation and the architecture of genomic landscapes remains elusive. For example, introgression between certain species might contribute to increased divergence and reproductive isolation between those species and other related species. In the end, a multispecies perspective on hybridization in combination with network approaches will lead to important insights into the history of life on this planet.</p
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Hybridization can serve as an evolutionary stimulus, but we have little understanding of introgression at early stages of hybrid zone formation. We analyze reproductive isolation and introgression between a range‐limited and a widespread species. Reproductive barriers are estimated based on differences in flowering time, ecogeographic distributions, and seed set from crosses. We find an asymmetrical mating barrier due to cytonuclear incompatibility that is consistent with observed clusters of coincident and concordant tension zone clines (barrier loci) for mtDNA haplotypes and nuclear SNPs. These groups of concordant clines are spread across the hybrid zone, resulting in weak coupling among barrier loci and extensive introgression. Neutral clines had nearly equal introgression into both species’ ranges, while putative cases of adaptive introgression had exceptionally wide clines with centers shifted towards one species. Analyses of cline shape indicate that secondary contact was initiated within the last 800 generations with the per‐generation dispersal between 200 and 400 meters, and provide some of the first estimates of the strength of selection required to account for observed levels of adaptive introgression. The weak species boundary between these species appears to be in early stages of dissolution, and ultimately will precipitate genetic swamping of the range‐limited species. This article is protected by copyright. All rights reserved
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Three distinct Canada jay (Perisoreus canadensis) morphotypes with easily recognizable plumage traits come into contact in western North America. Recent work demonstrated high genetic structure across the species’ range; however, patterns of genetic variation in these contact zones remain unknown. We categorized 605 individuals into one of three morphotypes (Pacific, Rocky Mountain, and Boreal) based on plumage, and genotyped individuals at the mtDNA control region and 12 microsatellite loci to assess the extent of hybridization between morphotypes. Our data showed cryptic genetic diversity and high cytonuclear discordance among morphotypes within contact zones, which is likely the result of recent and historical admixture. The distributions of the Boreal and Pacific morphotypes each showed a strong association with a single, distinct genetic group, whereas the Rocky Mountain morphotype exhibited higher genetic diversity and was associated with multiple genotypes. Our analyses show the importance of considering both plumage and genetic traits when examining contact zones between closely related taxa. Finally the data presented in this study reaffirm that the Pacific morphotype is distinct from the Boreal and Rocky Mountain morphotypes based on genetic, phenotypic and ecological data, indicating that the Pacific morphotype should be re-elevated to a full species.
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Hybridization and introgression can have complex consequences for both species evolution and conservation. Here, we investigated the origin and characteristics of a putative hybrid zone between two South American poison dart frog species, O. anchicayensis and the critically endangered O. lehmanni, which are heavily sought after on the illegal pet market. Using a combination of phenotypic (49 traits) and genomic (ddRADseq) data, we found that the putative hybrids are morphologically distinct from their parental species and confirmed genomic signatures of admixture in these populations. Several lines of evidence (hybrid indices, interspecific hybrid heterozygosity, genomic clines, comparisons with simulated hybrids and demographic modelling) support the conclusion that these populations are not comprised of early‐generation hybrids and thus, they likely did not arise as a result of illegal translocations associated with wildlife trafficking. Instead, they likely represent an independent lineage which has persisted through isolation and has only relatively recently re‐established gene flow with both parental species. Furthermore, we detected signals of differential introgression from parental species into these hybrid populations which suggest relaxed stabilizing selection on these aposematic color morphs, potentially via context‐dependent female choice. These populations thus provide a fascinating window into the role of hybridization, isolation and female choice in the diversification of South American poison dart frogs. In addition, our results underline the importance of landscape conservation measures to protect, not only known localities of nominal species, but also the phenotypic and genomic variation harbored by admixed lineages which represent crucial repositories for the impressive diversity in this system.
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Three species of closely related woodpeckers (sapsuckers; Sphyrapicus) hybridize where they come into contact, presenting a rare 'λ-shape' meeting of hybrid zones. Two of the three arms of this hybrid zone are located on either side of the Interior Plateau of British Columbia, Canada bordering the foothills of the Coast Mountains and the Rocky Mountains. The third arm is located in the eastern foothills of the Rocky Mountains. The zones of hybridization present high variability of phenotypes and alleles in relatively small areas and provide an opportunity to examine levels of reproductive isolation between the taxa involved. We examined phenotypes (morphometric traits and plumage) and genotypes of 175 live birds across the two hybrid zones. We used the Genotyping By Sequencing (GBS) method to identify 180 partially diagnostic single nucleotide polymorphisms (SNPs) to generate a genetic hybrid index (GHI) for each bird. Phenotypically diverged S. ruber and S. nuchalis are genetically closely related, while S. nuchalis and S. varius have similar plumage but are well separated at the genetic markers studied. The width of both hybrid zones is narrower than expected under neutrality, and analyses of both genotypes and phenotypes indicate that hybrids are rare in the hybrid zone. Rarity of hybrids indicates assortative mating and/or some form of fitness reduction in hybrids, which might maintain the species complex despite close genetic distance and introgression. These findings further support the treatment of the three taxa as distinct species. Journal of Avian Biology
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Hybrid zones have been promoted as windows on the evolutionary process and as laboratories for studying divergence and speciation. Patterns of divergence between hybridizing species can now be characterized on a genome-wide scale, and recent genome scans have focused on the presence of "islands" of divergence. Patterns of heterogeneous genomic divergence may reflect differential introgression following secondary contact and provide insights into which genome regions contribute to local adaptation, hybrid unfitness, and positive assortative mating. However, heterogeneous genome divergence can also arise in the absence of any gene flow, as a result of variation in selection and recombination across the genome. We suggest that to understand hybrid zone origins and dynamics, it is essential to distinguish between genome regions that are divergent between pure parental populations and regions that show restricted introgression where these populations interact in hybrid zones. The latter, more so than the former, reveal the likely genetic architecture of reproductive isolation. Mosaic hybrid zones, because of their complex structure and multiple contacts, are particularly good subjects for distinguishing primary intergradation from secondary contact. Comparisons among independent hybrid zones or transects that involve the "same" species pair can also help to distinguish between divergence with gene flow and secondary contact. However, data from replicate hybrid zones or replicate transects do not reveal consistent patterns; in a few cases, patterns of introgression are similar across independent transects, but for many taxa, there is distinct lack of concordance, presumably due to variation in environmental context and/or variation in the genetics of the interacting populations. This article is protected by copyright. All rights reserved.
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Speciation is a continuous and dynamic process, and studying organisms during the early stages of this process can aid in identifying speciation mechanisms. The mallard (Anas platyrhynchos) and Mexican duck (A. [p.] diazi) are two recently diverged taxa with a history of hybridization and controversial taxonomy. To understand their evolutionary history, we conducted genomic scans to characterize patterns of genetic diversity and divergence across the mitochondrial DNA (mtDNA) control region, 3523 autosomal loci, and 172 Z-linked sex chromosome loci. Between the two taxa, Z-linked loci (ΦST = 0.088) were 5.2 times more differentiated than autosomal DNA (ΦST = 0.017) but comparable to mtDNA (ΦST = 0.092). This elevated Z-differentiation deviated from neutral expectations inferred from simulated data that incorporated demographic history and differences in effective population sizes between marker types. Furthermore, 3% of Z-linked loci, compared to <0.1% of autosomal loci, were detected as outlier loci under divergent selection with elevated relative (ΦST ) and absolute (dXY ) estimates of divergence. In contrast, the ratio of Z-linked and autosomal differentiation among the seven Mexican duck sampling locations was close to 1:1 (ΦST = 0.018 for both markers). We conclude that between mallards and Mexican ducks, divergence at autosomal markers is largely neutral, whereas greater divergence on the Z-chromosome (or some portions thereof) is likely the product of selection that has been important in speciation. Our results contribute to a growing body of literature indicating elevated divergence on the Z chromosome and its likely importance in avian speciation. This article is protected by copyright. All rights reserved.
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We describe a model-based clustering method for using multilocus genotype data to infer population structure and assign individuals to populations. We assume a model in which there are K populations (where K may be unknown), each of which is characterized by a set of allele frequencies at each locus. Individuals in the sample are assigned (probabilistically) to populations, or jointly to two or more populations if their genotypes indicate that they are admixed. Our model does not assume a particular mutation process, and it can be applied to most of the commonly used genetic markers, provided that they are not closely linked. Applications of our method include demonstrating the presence of population structure, assigning individuals to populations, studying hybrid zones, and identifying migrants and admixed individuals. We show that the method can produce highly accurate assignments using modest numbers of loci—e.g., seven microsatellite loci in an example using genotype data from an endangered bird species. The software used for this article is available from http://www.stats.ox.ac.uk/~pritch/home.html.
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Hybridization among diverging lineages is common in nature. Genomic data provide a special opportunity to characterize the history of hybridization and the genetic basis of speciation. We review existing methods and empirical studies to identify recent advances in the genomics of hybridization, as well as issues that need to be addressed. Notable progress has been made in the development of methods for detecting hybridization and inferring individual ancestries. However, few approaches reconstruct the magnitude and timing of gene flow, estimate the fitness of hybrids, or incorporate knowledge of recombination rate. Empirical studies indicate that the genomic consequences of hybridization are complex, including a highly heterogeneous landscape of differentiation. Inferred characteristics of hybridization differ substantially among species groups. Loci showing unusual patterns - which may contribute to reproductive barriers - are usually scattered throughout the genome, with potential enrichment in sex chromosomes and regions of reduced recombination. We caution against the growing trend of interpreting genomic variation in summary statistics across genomes as evidence of differential gene flow. We argue that converting genomic patterns into useful inferences about hybridization will ultimately require models and methods that directly incorporate key ingredients of speciation, including the dynamic nature of gene flow, selection acting in hybrid populations, and recombination rate variation. This article is protected by copyright. All rights reserved.
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Under allopatric speciation, geographic barriers eliminate gene flow between eventual species at all loci in the genome simultaneously. There is increasing evidence, however, that speciation can be complex, with some loci experiencing gene flow during speciation or during bouts of secondary contact. In taxa with heteromorphic sex chromosomes-birds, butterflies, mammals, and Drosophila-the X (or Z) chromosome generally shows reduced levels of gene flow compared to autosomes. To investigate why, we develop population genetic models of secondary contact and gene flow at a neutral locus that is genetically linked to selected loci involved in hybrid incompatibilities and/or local adaptation. Using models that assume weak migration and strong selection, we compare gene flow at X-linked versus autosomal neutral loci as a function of linkage, dominance, sex-specific selection, and sex-specific recombination. For most cases, gene flow at neutral loci on the X is reduced relative to autosomes, as the greater efficacy of hemizygous selection in XY hybrids reduces the opportunity for neutral migrant alleles to escape their genetically linked, locally disfavored alleles via recombination. There are some circumstances, however, involving sex-limited selection and sex-limited recombination that allow neutral loci on the X to introgress more readily than those on autosomes.