Range-Wide Phylogeography and Ecological Niche Modeling Provide Insights into the Evolutionary History of the Mongolian Racerunner (Eremias argus) in Northeast Asia

Simple Summary: The Mongolian racerunner (Eremias argus) is a genetically diverse species with a wide distribution across Northeast Asia. The present study is the first to assess the genetic variation in E. argus across its entire geographic range using newly generated mtDNA cyt b and previously published data. We show the complex genetic pattern of this species, where most genetic divergence is not associated with geographic regions. This pattern is the result of multiple influences-robust dispersal ability resulting from ecological features, anthropogenic influence of translocation, and past climate change. Geographic distance has primarily shaped the genetic structure of the species, as indicated by a strong pattern of isolation by distance across all populations. The population growth of E. argus from the Last Interglacial to the Last Glacial Maximum is likely a consequence of an increase in favorable habitats with mild climates following the development of monsoons in East Asia since the mid-Late Pleistocene. Overall, the population genetic structure of E. argus was likely driven by a combination of climatic and geographic changes rather than direct ice sheet coverage. Our results highlight the importance of combining genetic approaches with environmental data when assessing the impact of Pleistocene climatic oscillations. The Mongolian racerunner, Eremias argus, is a small lizard endemic to Northeast Asia that can serve as an excellent model for investigating how geography and past climate change have jointly influenced the evolution of biodiversity in this region. To elucidate the processes underlying its diversification and demography, we reconstructed the range-wide phylogeographic pattern and evolutionary trajectory, using phylogenetic, population genetic, landscape genetic, Bayesian phylogeographic reconstruction and ecological niche modeling approaches. Phylogenetic analyses of the mtDNA cyt b gene revealed eight lineages that were unbounded by geographic region. The genetic structure of E. argus was mainly determined by geographic distance. Divergence dating indicated that E. argus and E. brenchleyi diverged during the Mid-Pliocene Warm Period. E. argus was estimated to have coalesced at similar to 0.4351 Ma (Marine Isotope Stage 19). Bayesian phylogeographic diffusion analysis revealed out-of-Inner Mongolia and rapid colonization events from the end of the Last Interglacial to the Last Glacial Maximum, which is consistent with the expanded suitable range of the Last Glacial Maximum. Pre-Last Glacial Maximum growth of population is presented for most lineages of E. argus. The Glacial Maximum contraction model and the previous multiple glacial refugia hypotheses are rejected. This may be due to an increase in the amount of climatically favorable habitats in Northeast Asia. Furthermore, E. argus barbouri most likely represents an invalid taxon. The present study is the first to report a range-wide phylogeography of reptiles over such a large region in Northeast Asia. Our results make a significant contribution towards understanding the biogeography of the entire Northeast Asia.