Asymmetric Introgression Research Articles

Genetic Divergence Across Glacial Refugia Despite Interglacial Gene Flow in a Crested Newt

MtDNA-based phylogeography has illuminated the impact of the Pleistocene Ice Age on species distribution dynamics and the build-up of genetic divergence. The well-known shortcomings of mtDNA in biogeographical inference can be compensated by integrating multilocus data and species distribution modelling into phylogeography. We re-visit the phylogeography of the Italian crested newt (Triturus carnifex), a species distributed in two of Europe’s main glacial refugia, the Balkan and Italian Peninsulas. While a new 51 nuclear DNA marker dataset supports the existence of three lineages previously suggested by mtDNA (Balkan, northern Italy and southern Italy), the nuclear DNA dataset also provides improved resolution where these lineages have obtained secondary contact. We observe geographically restricted admixture at the contact between the Balkan and northern Italy gene pools and identify a potential mtDNA ghost lineage here. At the contact between the northern and southern Italy gene pools we find admixture over a broader area, as well as asymmetric mtDNA introgression. Our species distribution model is in agreement with a distribution restricted to distinct refugia during Pleistocene glacial cycles and postglacial expansion with secondary contact. Our study supports: (1) the relevance of the north-western Balkan Peninsula as a discrete glacial refugium; (2) the importance of north-eastern Italy and the northern Apennine as suture zones; and (3) the applicability of a refugia-within-refugia scenario within the Italian Peninsula.

How do species barriers decay? Concordance and local introgression in mosaic hybrid zones of mussels.

The Mytilus complex of marine mussel species forms a mosaic of hybrid zones, found across temperate regions of the globe. This allows us to study 'replicated' instances of secondary contact between closely related species. Previous work on this complex has shown that local introgression is both widespread and highly heterogeneous, and has identified SNPs that are outliers of differentiation between lineages. Here, we developed an ancestry-informative panel of such SNPs. We then compared their frequencies in newly sampled populations, including samples from within the hybrid zones, and parental populations at different distances from the contact. Results show that close to the hybrid zones, some outlier loci are near to fixation for the heterospecific allele, suggesting enhanced local introgression, or the local sweep of a shared ancestral allele. Conversely, genomic cline analyses, treating local parental populations as the reference, reveal a globally high concordance among loci, albeit with a few signals of asymmetric introgression. Enhanced local introgression at specific loci is consistent with the early transfer of adaptive variants after contact, possibly including asymmetric bi-stable variants (Dobzhansky-Muller incompatibilities), or haplotypes loaded with fewer deleterious mutations. Having escaped one barrier, however, these variants can be trapped or delayed at the next barrier, confining the introgression locally. These results shed light on the decay of species barriers during phases of contact.

Dispersal as a result of asymmetrical hybridization between two closely related oak species in China

Hybridization has played an important role in plant evolution. Less attention has been paid, however, to its role in dispersal. In this study, historical divergence and hybridization were investigated in two closely related Chinese oaks, Quercus mongolica and Q. liaotungensis, to estimate the role that hybridization played in their dispersal. We genotyped 27 Q. mongolica and Q. liaotungensis populations throughout the distributional range of the two oak species, using 14 single-copy nuclear genes and four noncoding chloroplast DNA regions. Bayesian cluster and population tree analyses indicated that there were three groups over all oak populations, namely, Q. mongolica, northwest–northern China (NW-NC) Q. liaotungensis, and northeastern China (NEC) Q. liaotungensis. Approximate Bayesian computation simulation supported an asymmetrical hybridization origin of NEC Q. liaotungensis, after a previous divergence between NW-NC Q. liaotungensis and Q. mongolica. IMa3 analyses suggested that Q. liaotungensis and Q. mongolica diverged in the NW-NC and NEC regions, respectively, and that NEC Q. liaotungensis arose from Q. mongolica, not from NW-NC Q. liaotungensis, and was greatly introgressed by NW-NC Q. liaotungensis. Oak populations in NW-NC and NEC regions held different chloroplast DNA haplotypes, and Q. liaotungensis in NEC shared most haplotypes with Q. mongolica populations, but none with NW-NC Q. liaotungensis populations, suggesting the maternal origin of NEC Q. liaotungensis from Q. mongolica. This study found clear signals of isolation divergence of Q. liaotungensis in NW-NC and Q. mongolica in NEC, and the results suggest that asymmetrical hybridization and introgression from Q. liaotungensis to Q. mongolica, mostly likely via pollen flow, facilitated Q. liaotungensis dispersal to NEC.

The evolution of strong reproductive isolation between sympatric intertidal snails.

The evolution of strong reproductive isolation (RI) is fundamental to the origins and maintenance of biological diversity, especially in situations where geographical distributions of taxa broadly overlap. But what is the history behind strong barriers currently acting in sympatry? Using whole-genome sequencing and single nucleotide polymorphism genotyping, we inferred (i) the evolutionary relationships, (ii) the strength of RI, and (iii) the demographic history of divergence between two broadly sympatric taxa of intertidal snail. Despite being cryptic, based on external morphology, Littorina arcana and Littorina saxatilis differ in their mode of female reproduction (egg-laying versus brooding), which may generate a strong post-zygotic barrier. We show that egg-laying and brooding snails are closely related, but genetically distinct. Genotyping of 3092 snails from three locations failed to recover any recent hybrid or backcrossed individuals, confirming that RI is strong. There was, however, evidence for a very low level of asymmetrical introgression, suggesting that isolation remains incomplete. The presence of strong, asymmetrical RI was further supported by demographic analysis of these populations. Although the taxa are currently broadly sympatric, demographic modelling suggests that they initially diverged during a short period of geographical separation involving very low gene flow. Our study suggests that some geographical separation may kick-start the evolution of strong RI, facilitating subsequent coexistence of taxa in sympatry. The strength of RI needed to achieve sympatry and the subsequent effect of sympatry on RI remain open questions. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.

Reproductive characteristics of two Triturus species (Amphibia: Caudata)

During three consecutive years, we compared the reproductive characteristics and oviposition dynamics of two crested newt species, Triturus ivanbureschi and T. macedonicus. These two well-defined species are of special interest because of complex interactions at their contact zone, which include hybridization, species replacement and asymmetric mitochondrial DNA introgression. In common garden experiments, females were introduced to conspecific males, to males of other species and to hybrid males. We monitored the total number and size of the deposited eggs, as well as the dynamics and duration of oviposition during three consecutive years. The number of deposited eggs of Triturus species was much higher than previously reported. Triturus macedonicus lay more eggs that were of larger size in comparison to T. ivanbureschi. Also, the onset of T. macedonicus oviposition was considerably delayed compared to T. ivanbureschi. These are fundamental data, important for understanding complex species interactions in their contact zones.

Discordant patterns of introgression across a narrow hybrid zone between two cryptic lineages of an Iberian endemic newt.

The study of natural hybrid zones can illuminate aspects of lineage divergence and speciation in morphologically cryptic taxa. We studied a hybrid zone between two highly divergent but morphologically similar lineages (south-western and south-eastern) of the Iberian endemic Bosca's newt (Lissotriton boscai) in SW Iberia with a multilocus dataset (microsatellites, nuclear and mitochondrial genes). STRUCTURE and NEWHYBRIDS analyses retrieved few admixed individuals, which classified as backcrosses involving parental individuals of the south-western lineage. Our results show asymmetric introgression of mtDNA beyond the contact from this lineage into the south-eastern lineage. Analysis of nongeographic introgression patterns revealed asymmetries in the direction of introgression, but except for mtDNA, we did not find evidence for nonconcordant introgression patterns across nuclear loci. Analysis of a 150-km transect across the hybrid zone showed broadly coincident cline widths (ca. 3.2-27.9km), and concordant cline centres across all markers, except for mtDNA that is displaced ca. 60km northward. Results from ecological niche modelling show that the hybrid zone is in a climatically homogenous area with suitable habitat for the species, suggesting that contact between the two lineages is unlikely to occur further south as their distributions are currently separated by an extensive area of unfavourable habitat. Taken together, our findings suggest the genetic structure of this hybrid zone results from the interplay of historical (biogeographic) and population-level processes. The narrowness and coincidence of genetic clines can be explained by weak selection against hybrids and reflect a degree of reproductive isolation that is consistent with cryptic speciation.

Variable outcomes of hybridization between declining Alosa alosa and Alosa fallax.

Hybridization dynamics between co‐occurring species in environments where human‐mediated changes take place are important to quantify for furthering our understanding of human impacts on species evolution and for informing management. The allis shad Alosa alosa (Linnaeus, 1758) and twaite shad Alosa fallax (Lacépède, 1803), two clupeids sister species, have been severely impacted by human activities across Europe. The shrinkage of A. alosa distribution range along with the decline of the remaining populations' abundance threatens its persistence. The main objective was to evaluate the extent of hybridization and introgression between those interacting species. We developed a set of 77 species‐specific SNP loci that allowed a better resolution than morphological traits as they enabled the detection of hybrids up to the third generation. Variable rates of contemporary hybridization and introgression patterns were detected in 12 studied sites across the French Atlantic coast. Mitochondrial markers revealed a cyto‐nuclear discordance almost invariably involving A. alosa individuals with an A. fallax mitochondrial DNA and provided evidence of historical asymmetric introgression. Overall, contemporary and historical introgression revealed by nuclear and mitochondrial markers strongly suggests that a transfer of genes occurs from A. fallax toward A. alosa genome since at least four generations. Moreover, the outcomes of introgression greatly depend on the catchments where local processes are thought to occur. Undoubtedly, interspecific interaction and gene flow should not be overlooked when considering the management of those species.

Genetic admixture despite ecological segregation in a North African sparrow hybrid zone (Aves, Passeriformes, Passer domesticus×Passer hispaniolensis).

Under different environmental conditions, hybridization between the same species might result in different patterns of genetic admixture. Particularly, species pairs with large distribution ranges and long evolutionary history may have experienced several independent hybridization events over time in different zones of overlap. In birds, the diverse hybrid populations of the house sparrow (Passer domesticus) and the Spanish sparrow (Passer hispaniolensis) provide a striking example. Throughout their range of sympatry, these two species do not regularly interbreed; however, a stabilized hybrid form (Passer italiae) exists on the Italian Peninsula and on several Mediterranean islands. The spatial distribution pattern on the Eurasian continent strongly contrasts the situation in North Africa, where house sparrows and Spanish sparrows occur in close vicinity of phenotypically intermediate populations across a broad mosaic hybrid zone. In this study, we investigate patterns of divergence and admixture among the two parental species, stabilized and nonstabilized hybrid populations in Italy and Algeria based on a mitochondrial marker, a sex chromosomal marker, and 12 microsatellite loci. In Algeria, despite strong spatial and temporal separation of urban early‐breeding house sparrows and hybrids and rural late‐breeding Spanish sparrows, we found strong genetic admixture of mitochondrial and nuclear markers across all study populations and phenotypes. That pattern of admixture in the North African hybrid zone is strikingly different from i) the Iberian area of sympatry where we observed only weak asymmetrical introgression of Spanish sparrow nuclear alleles into local house sparrow populations and ii) the very homogenous Italian sparrow population where the mitogenome of one parent (P. domesticus) and the Z‐chromosomal marker of the other parent (P. hispaniolensis) are fixed. The North African sparrow hybrids provide a further example of enhanced hybridization along with recent urbanization and anthropogenic land‐use changes in a mosaic landscape.

Mixing Genetically and Morphologically Distinct Populations in Translocations: Asymmetrical Introgression in A Newly Established Population of the Boodie (Bettongia lesueur).

The use of multiple source populations provides a way to maximise genetic variation and reduce the impacts of inbreeding depression in newly established translocated populations. However, there is a risk that individuals from different source populations will not interbreed, leading to population structure and smaller effective population sizes than expected. Here, we investigate the genetic consequences of mixing two isolated, morphologically distinct island populations of boodies (Bettongia lesueur) in a translocation to mainland Australia over three generations. Using 18 microsatellite loci and the mitochondrial D-loop region, we monitored the released animals and their offspring between 2010 and 2013. Despite high levels of divergence between the two source populations (FST = 0.42 and ϕST = 0.72), there was clear evidence of interbreeding between animals from different populations. However, interbreeding was non-random, with a significant bias towards crosses between the genetically smaller-sized Barrow Island males and the larger-sized Dorre Island females. This pattern of introgression was opposite to the expectation that male–male competition or female mate choice would favour larger males. This study shows how mixing diverged populations can bolster genetic variation in newly established mammal populations, but the ultimate outcome can be difficult to predict, highlighting the need for continued genetic monitoring to assess the long-term impacts of admixture.

Hybridization drives genetic erosion in sympatric desert fishes of western North America.

Many species have evolved or currently coexist in sympatry due to differential adaptation in a heterogeneous environment. However, anthropogenic habitat modifications can either disrupt reproductive barriers or obscure environmental conditions which underlie fitness gradients. In this study, we evaluated the potential for an anthropogenically-mediated shift in reproductive boundaries that separate two historically sympatric fish species (Gila cypha and G. robusta) endemic to the Colorado River Basin using ddRAD sequencing of 368 individuals. We first examined the integrity of reproductive isolation while in sympatry and allopatry, then characterized hybrid ancestries using genealogical assignment tests. We tested for localized erosion of reproductive isolation by comparing site-wise genomic clines against global patterns and identified a breakdown in the drainage-wide pattern of selection against interspecific heterozygotes. This, in turn, allowed for the formation of a hybrid swarm in one tributary, and asymmetric introgression where species co-occur. We also detected a weak but significant relationship between genetic purity and degree of consumptive water removal, suggesting a role for anthropogenic habitat modifications in undermining species boundaries or expanding historically limited introgression. In addition, results from basin-wide genomic clines suggested that hybrids and parental forms are adaptively nonequivalent. If so, then a failure to manage for hybridization will exacerbate the long-term extinction risk in parental populations. These results reinforce the role of anthropogenic habitat modification in promoting interspecific introgression in sympatric species by relaxing divergent selection. This, in turn, underscores a broader role for hybridization in decreasing global biodiversity within rapidly deteriorating environments.

Conservation implications of asymmetric introgression and reproductive barriers in a rare primrose species

BackgroundPrimula is a large genus of flowering herbs well known for their heterostyly. Currently few natural hybrids are known and reproductive barriers in this genus in the wild have received little attention. However, there is instance of hybridization between rare and widely-spread species, and conservation implications of such situation is poorly understood. In the present study, we investigated hybridization patterns and reproductive barriers between a wide spread species, Primula poissonii and a rare species P. anisodora, of which only three populations are currently known.ResultsPollinator-mediated reproductive isolation was strong between parental species but not significant between hybrids and parental species. Hand pollination experiments showed significant reduction of both fruit- and seed-set for heterospecific pollination as compared with conspecific pollination for both parental species. Furthermore, hybrids had higher fruit- and seed-set when pollinated with P. anisodora pollen as opposed to P. poissonii pollen. Microsatellites identified backcrosses to P. anisodora in two of the three populations of P. anisodora, and additionally more individuals of P. anisodora showed introgression from P. poissonii than vice versa.ConclusionsThese results provide evidence for potential genetic swamping of the P. anisodora populations, which could pose a serious threat for this locally endemic species.

Homoploid hybridization of plants in the Hengduan mountains region.

The Hengduan Mountains Region (HMR) is a major global biodiversity hotspot. Complex tectonic and historical climatic conditions created opportunities for natural interspecific hybridization. Likewise, anthropogenic disturbance potentially raises the frequency of hybridization. Among species studies to date, the frequency of homoploid hybridization appears in the HMR. Of nine taxa in which natural hybridization has been detected, three groups are involved in homoploid hybrid speciation, and species pairs from the remaining six genera suggest that continuous gene flow occurs in hybrid zones. Reproductive isolation may greatly affect the dynamic and architecture of hybrid zones in the HMR. Asymmetrical hybridization and introgression can primarily be attributed to both prezygotic and postzygotic barriers. The frequent observation of such asymmetry may imply that reproductive barrier contributes to maintaining species boundaries in the alpine region. Ecological isolations with environmental disturbance may promote breeding barriers between parental species and hybrids. Hybrid zones may be an important phase for homoploid hybrid speciation. Hybrid zones potentially provided abundant genetic resources for the diversification of the HMR flora. The ecological and molecular mechanisms of control and mediation for natural hybridization will help biologists to understand the formation of biodiversity in the HMR. More researches from ecological and molecular aspects were required in future studies.

Genomic and phenotypic consequences of two independent secondary contact zones between allopatric lineages of the anadromous ice goby Leucopsarion petersii.

Genetic and phenotypic analyses of independent secondary contact zones between certain pairs of divergent populations offer powerful opportunities to assess whether the consequences vary with different environmental backgrounds. Populations of the ice goby Leucopsarion petersii are distributed throughout the Japanese archipelago and comprise genetically and phenotypically divergent groups in the Japan Sea and the Pacific Ocean. In particular, populations in the Japan Sea have a larger body size and numbers of vertebrae than those in the Pacific Ocean. Herein, we performed integrated analyses of genotypes and phenotypes of two independent secondary contact zones and investigated their consequences. Population genetic analyses revealed asymmetric introgression of the mitochondrial genome of either lineage relative to little admixture of nuclear genomes in both secondary contact zones. On phenotype analyses, vertebral numbers were clearly explained by nuclear genomic ancestry in both secondary contact zones, whereas body size was not, suggesting that a little introgression of nuclear genes regulates body size. Actually, we observed biased introgression of a candidate gene, neuropeptide Y (NPY), which potentially controls body size in the ice goby. Moreover, the body size changes in the introgressed populations possibly affect the introgression patterns of mitochondrial genomes across these zones. Collectively, our results demonstrated that genomic and phenotypic consequences of secondary contact varied in marine variable environments.

Testing an hypothesis of hybrid zone movement for toads in France.

Hybrid zone movement may result in substantial unidirectional introgression of selectively neutral material from the local to the advancing species, leaving a genetic footprint. This genetic footprint is represented by a trail of asymmetric tails and displaced cline centres in the wake of the moving hybrid zone. A peak of admixture linkage disequilibrium is predicted to exist ahead of the centre of the moving hybrid zone. We test these predictions of the movement hypothesis in a hybrid zone between common (Bufo bufo) and spined toads (B.spinosus), using 31 nuclear and one mtDNA SNPs along a transect in the northwest of France. Average effective selection in Bufo hybrids is low and clines vary in shape and centre. A weak pattern of asymmetric introgression is inferred from cline discordance of seven nuclear markers. The dominant direction of gene flow is from B.spinosus to B.bufo and is in support of southward movement of the hybrid zone. Conversely, a peak of admixture linkage disequilibrium north of the hybrid zone suggests northward movement. These contrasting results can be explained by reproductive isolation of the B.spinosus and B.bufo gene pools at the southern (B.spinosus) side of the hybrid zone. The joint occurrence of asymmetric introgression and admixture linkage disequilibrium can also be explained by the combination of low dispersal and random genetic drift due to low effective population sizes.

Differential introgression of a female competitive trait in a hybrid zone between sex-role reversed species.

Mating behavior between recently diverged species in secondary contact can impede or promote reproductive isolation. Traditionally, researchers focus on the importance of female mate choice and male-male competition in maintaining or eroding species barriers. Although female-female competition is widespread, little is known about its role in the speciation process. Here, we investigate a case of interspecific female competition and its influence on patterns of phenotypic and genetic introgression between species. We examine a hybrid zone between sex-role reversed, Neotropical shorebird species, the northern jacana (Jacana spinosa) and wattled jacana (J. jacana), in which female-female competition is a major determinant of reproductive success. Previous work found that females of the more aggressive and larger species, J. spinosa, disproportionately mother hybrid offspring, potentially by monopolizing breeding territories in sympatry with J. jacana. We find a cline shift of female body mass relative to the genetic center of the hybrid zone, consistent with asymmetric introgression of this competitive trait. We suggest that divergence in sexual characteristics between sex-role reversed females can influence patterns of gene flow upon secondary contact, similar to males in systems with more typical sex roles.

Asymmetric introgression between fishes in the Red River basin of Texas is associated with variation in water quality.

When ecologically divergent taxa encounter one another, hybrid zones can form when reproductive isolation is incomplete. The location of such hybrid zones can be influenced by environmental variables, and an ecological context can provide unique insights into the mechanisms by which species diverge and are maintained. Two ecologically differentiated species of small benthic fishes, the endemic and imperiled prairie chub, Macrhybopsis australis, and the shoal chub, Macrhybopsis hyostoma, are locally sympatric within the upper Red River Basin of Texas. We integrated population genomic data and environmental data to investigate species divergence and the maintenance of species boundaries in these two species. We found evidence of advanced‐generation asymmetric hybridization and introgression, with shoal chub alleles introgressing more frequently into prairie chubs than the reciprocal. Using a Bayesian Genomic Cline framework, patterns of genomic introgression were revealed to be quite heterogeneous, yet shoal chub alleles were found to have likely selectively introgressed across species boundaries significantly more often than prairie chub alleles, potentially explaining some of the observed asymmetry in hybridization. These patterns were remarkably consistent across two sampled geographic regions of hybridization. Several environmental variables were found to significantly predict individual admixture, suggesting ecological isolation might maintain species boundaries.

Coexistence of two sympatric cryptic bat species in French Guiana: insights from genetic, acoustic and ecological data

BackgroundThe distinction between lineages of neotropical bats from the Pteronotus parnellii species complex has been previously made according to mitochondrial DNA, and especially morphology and acoustics, in order to separate them into two species. In these studies, either sample sizes were too low when genetic and acoustic or morphological data were gathered on the same individuals, or genetic and other data were collected on different individuals. In this study, we intensively sampled bats in 4 caves and combined all approaches in order to analyse genetic, morphologic, and acoustic divergence between these lineages that live in the same caves in French Guiana.ResultsA multiplex of 20 polymorphic microsatellite markers was developed using the 454-pyrosequencing technique to investigate for the first time the extent of reproductive isolation between the two lineages and the population genetic structure within lineages. We genotyped 748 individuals sampled between 2010 and 2015 at the 20 nuclear microsatellite loci and sequenced a portion of the cytochrome c oxydase I gene in a subset of these. Two distinct, non-overlapping haplogroups corresponding to cryptic species P. alitonus and P. rubiginosus were revealed, in accordance with previous findings. No spatial genetic structure between caves was detected for both species. Hybridization appeared to be quite limited (0.1–4%) using microsatellite markers whereas introgression was more common (7.5%) and asymmetric for mitochondrial DNA (mtDNA).ConclusionsThe extremely low rate of hybridization could be explained by differences in life cycle phenology between species as well as morphological and acoustical distinction between sexes in one or the other species. Taken together, these results add to our growing understanding of the nature of species boundaries in Pteronotus parnelli, but deserve more in-depth studies to understand the evolutionary processes underlying asymmetric mtDNA introgression in this group of cryptic species.

Implications of introgression for wildlife translocations: the case of North American martens

The evolutionary consequences of natural introgression provide a rare opportunity to retrospectively evaluate how the introduction of exotics or genetic rescue efforts may impact endemic faunas. Phylogeographic structure among mainland, endemic insular, and introduced North American marten (Martes americana and M. caurina) populations have been shaped by a complex history of natural, post-glacial population expansion followed by a series of anthropogenic introductions. In some cases, both natural colonization and translocations facilitated secondary contact, offering a series of replicated experiments that demonstrate how introgression, in these cases following isolation (insular and refugial), shapes genetic diversity. We test whether genetic exchange is occurring between North American marten species using mitochondrial genomes and ten nuclear loci. We present evidence of biased nuclear introgression from M. caurina into M. americana across two natural hybrid zones (insular and mainland) and found no remnant evidence of M. caurina on islands that received M. americana translocations, suggesting prior absence, potential extirpation, or genetic swamping of M. caurina from these islands. Our results highlight the importance of understanding phylogeographic variation prior to identifying source populations for wildlife translocations and caution the use of genetic rescue for North American marten populations. Although previously managed as a single species, these two species show substantial genetic divergence. When the two are placed into contact, they exhibit unidirectional, asymmetric introgression with potentially negative consequences for M. caurina, underscoring the value of mindful consideration of introgression in wildlife management.

Maladaptive secondary sexual characteristics reduce the reproductive success of hybrids between native and non-native salmonids.

Human‐mediated hybridization between introduced and native species is one of the most serious threats to native taxa. Although field studies have attempted to quantify the relative fitness or reproductive success of parental species and their hybrids, only a few studies have unraveled the factors determining the fitness of hybrids. Here, we hypothesized that maladaptive secondary sexual characteristics may reduce fitness of hybrids between two fish species. To test this, we evaluated the reproductive success of introduced brook trout (BT: Salvelinus fontinalis), native white‐spotted charr (WSC: S. leucomaenis) and their hybrids in a natural stream in Hokkaido, Japan, where the two parental species show remarkably different male secondary sexual characteristics, such as elongated jaws and deeper bodies. We predicted that introgression from WSC is maladaptive for BT males because the BT male has more prominent secondary sexual characteristics. Our results suggest that both sexual selection and outbreeding depression in males and females significantly influence an individual's reproductive success. Our results also suggest that asymmetric introgression may increase the risks to persistence in the recipient species.

Genomic evidence for asymmetric introgression by sexual selection in the common wall lizard.

Strongly selected characters can be transferred from one lineage to another with limited genetic exchange, resulting in asymmetric introgression and a mosaic genome in the receiving population. However, systems are rarely sufficiently well studied to link the pattern of introgression to its underlying process. Male common wall lizards in western Italy exhibit exaggeration of a suite of sexually selected characters that make them outcompete males from a distantly related lineage that lack these characters. This results in asymmetric hybridization and adaptive introgression of the suite of characters following secondary contact. We developed genomewide markers to infer the demographic history of gene flow between different genetic lineages, identify the spread of the sexually selected syndrome, and test the prediction that introgression should be asymmetric and heterogeneous across the genome. Our results show that secondary contact was accompanied by gene flow in both directions across most of the genome, but with approximately 3% of the genome showing highly asymmetric introgression in the predicted direction. Demographic simulations reveal that this asymmetric gene flow is more recent than the initial secondary contact, and the data suggest that the exaggerated male sexual characters originated within the Italian lineage and subsequently spread throughout this lineage before eventually reaching the contact zone. These results demonstrate that sexual selection can cause a suite of characters to spread throughout both closely and distantly related lineages with limited gene flow across the genome at large.