Geography and past climate changes have shaped the evolution of a widespread lizard in arid Central Asia

Abstract

The complex orogenic history and structure of Central Asia, coupled with Pleistocene glacial cycles have generated its stepwise aridification. Such events would have significantly influenced the evolution of many mid-latitude species in arid Central Asia (ACA). In this study, we employed two mitochondrial genes (CO1 and ND2) and genome-wide SNPs, coupled with ecological niche modeling, to investigate the lineage diversification and historical demography within a widespread lizard Phrynocephalus helioscopus, and their associations with geography and past climate change. We obtained the mtDNA dataset for 300 individuals from 96 localities within the known range of the lizard, among which 51 individuals from 27 localities were selected for generating the SNP dataset via the genotyping-by-sequencing approach. Phylogenetic analyses of the concatenated mtDNA dataset revealed eight geographically correlated lineages that diverged by 4.21–10.41% for the CO1 gene, which were estimated to have coalesced ∼4.47 million years ago. However, we observed mito-nuclear discordance pattern regarding the population of Clade V (P. helioscopus sergeevi) from Tajikistan. Ancestral area estimations suggested that P. helioscopus originated from the Fergana Valley and then dispersed into the adjacent areas in ACA along with a history of multiple allopatric divergence processes, suggesting that Fergana may have been the cradle of diversification of P. helioscopus. The intensification of aridification across Central Asia during the Late Pliocene may have facilitated the rapid radiation of this arid-adapted lizard throughout this vast territory. Subsequently, the geological events (e.g., uplift of the Hissar-Alay, transgressions of the Caspian Sea) and geographic barriers (e.g., Amu Darya River, Zeravshan River) during the Pleistocene triggered the progressive diversification of P. helioscopus. Interestingly, Clade VIII (P. helioscopus varius) experienced rapid population growth coupled with range expansion while Clade IV (P. helioscopus cameranoi) underwent drastic population expansion associated with range contraction during the Last Glacial Maximum. In Clade IV, but not in Clade VIII, environmental turnover contributes more to mitochondrial genetic distinctiveness than geographic distance. Overall, the SNP dataset demonstrates that geographic distance plays a greater role than environmental distance. Both the mtDNA dataset and the SNP dataset suggest local-scale genetic differentiation in Clade IV and Clade VIII, revealing potential geographic barriers in the Ili River Valley and the Junggar Basin, respectively. Twenty-seven outlier SNPs associated with environmental factors (precipitation and temperature) were identified, which supports the signature of local adaptation to the arid desert environment. Finally, our finding suggests taxonomic implications, such as support for full species status for P. saidalievi (Clade II) and P. meridionalis (Clade I). Future analyses based on further evidence and increased taxon and geographic sampling should be carried out to corroborate our findings.