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.

BackgroundUnderstanding how organisms adapt to high-elevation environments at a genome scale provides novel insights into the process of adaptive evolution. Previous studies have mainly focused on endothermic organisms, while poikilothermic species may have evolved different mechanisms to cope with high-elevation environments. In this context, we sequenced transcriptomes of a pair of closely related anuran species, Rana chensinensis and R. kukunoris, which inhabit respective low- and high-elevation habitats. By comparing the two transcriptomes, we identified candidate genes that may be involved in high-elevation adaption in poikilothermic species.ResultsOver 66 million sequence reads from each transcriptome were generated. A total of 41,858 and 39,293 transcripts for each species were obtained by de novo assembly. By comparing the orthologous transcripts, we identified 125 protein-coding genes that have likely experienced strong positive selection (Ka/Ks>1). In addition, 335 genes that may bear a signature of positive selection (1≥Ka/Ks>0.5) were also recognized. By considering their functions, fourteen candidate genes were determined to be likely involved in high-elevation adaptation, including two CYP genes, USP-1, and several others.ConclusionsWe identified a set of candidate genes that may have promoted adaptation of R. kukunoris to its high-elevation environment. These include several genes that have previously been associated with oxygen binding, response to UV radiation, and repair of free radical injury. Detailed molecular, physiological, and phenotypic studies are required to better understand the roles of these genes in improving the performance of R. kukunoris in a high-elevation environment. We have evidence for both convergent and divergent evolution between endothermic and poikilothemic species, but additional research across a wide range of organisms will be necessary to comprehend the complexity of high-elevation adaptation.

The Mediterranean basin is a hotspot of biodiversity, fuelled by climatic oscillation and geological change over the past 20 million years. Wall lizards of the genus Podarcis are among the most abundant, diverse, and conspicuous Mediterranean fauna. Here, we unravel the remarkably entangled evolutionary history of wall lizards by sequencing genomes of 34 major lineages covering 26 species. We demonstrate an early (>11 MYA) separation into two clades centred on the Iberian and Balkan Peninsulas, and two clades of Mediterranean island endemics. Diversification within these clades was pronounced between 6.5–4.0 MYA, a period spanning the Messinian Salinity Crisis, during which the Mediterranean Sea nearly dried up before rapidly refilling. However, genetic exchange between lineages has been a pervasive feature throughout the entire history of wall lizards. This has resulted in a highly reticulated pattern of evolution across the group, characterised by mosaic genomes with major contributions from two or more parental taxa. These hybrid lineages gave rise to several of the extant species that are endemic to Mediterranean islands. The mosaic genomes of island endemics may have promoted their extraordinary adaptability and striking diversity in body size, shape and colouration, which have puzzled biologists for centuries.