Genomic insights into the reticulate evolution of viviparous Phrynocephalus lizards on the Qinghai-Tibetan Plateau

The contribution of hybridization to the speciation and diversification of organisms remains a topic of ongoing debate. While ancient reticulate events have been increasingly recognized as a common feature in evolutionary history of many species, the role of hybridization in driving adaptation, especially in extreme environments, is still unclear. The viviparous Phrynocephalus lizards present an excellent system to investigate this question, which are distributed across the Qinghai-Tibetan Plateau (QTP) with most species occurring above 2,300 m above sea level. In this study, we employed an integrative approach combining population genetics, phylogenomics and gene flow assessment to unravel the evolutionary history of this clade using genome-wide dataset. Our results revealed a robust phylogenetic relationship between these species with evidence of multiple reticulate events throughout their colonization to the challenging QTP environments. Notably, we found the two highest-altitude species, P. erythrurus and P. theobaldi, received approximately 41% and 14% of their alleles via interspecific gene flow, respectively. Coding genes in these introgressed regions exhibited significantly accelerated evolution, and were over-represented in functions such as “response to temperature stimulus” and “circulatory system process”, including key genes such as ACE and VEGFC, potentially facilitating their adaptation to high-altitude environments. This study suggests the broader relevance of gene flow in shaping evolutionary trajectories of species in extreme environments, and provides novel insights into the understanding of natural hybridization.