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

Abstract

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.

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

“…Considering that female J. spinosa are larger in morphological traits used in competition and more aggressive than female J. jacana (Lipshutz 2017b), our results are consistent with the hypothesis that female competition influences patterns of introgression between the jacana species. Our findings align with studies of other hybrid zones (Baldassarre et al 2014;Yang et al 2018) in which traits under selection by either female choice or male competition introgress asymmetrically relative to the genome-wide cline center between species.…”

“…; Yang et al. ). An asymmetry in competitive ability can also facilitate hybrid zone movement via geographical displacement (Grava et al.…”

“…; Yang et al. ) in which traits under selection by either female choice or male competition introgress asymmetrically relative to the genome‐wide cline center between species.…”

“…A number of empirical studies suggest that asymmetry in competitive ability can facilitate differential introgression between lineages (reviewed in Lipshutz 2017a; Tinghitella et al 2018). One case study example is a hybrid zone between subspecies of the common wall lizard (Podarcis muralis), in which asymmetries in male dominance lead to directional hybridization (MacGregor et al 2017) and asymmetric introgression (While et al 2015;Yang et al 2018). An asymmetry in competitive ability can also facilitate hybrid zone movement via geographical displacement (Grava et al 2012).…”

Evolutionary and demographic correlates of Pleistocene coastline changes in the Sicilian wall lizardPodarcis wagleriana

“…Strong evidence for asymmetric nuclear introgression between intraspecific lineages, following secondary contact, has been recently provided for the common wall lizard Podarcis muralis (While et al., ; Yang et al., ). In this species, strong asymmetries in male competitive ability and mating success between lineages originated in distinct glacial refugia explains the pattern of asymmetric hybridization upon secondary contact, with the replacement of nuclear characters of the subdominant lineage (While et al., ).…”