Genetic Structure and Population History of the Zaisan Toad-Headed Agama (Phrynocephalus melanurus) Inferred from Mitochondrial DNA

Simple Summary The effects of Quaternary climatic oscillations on lineage diversification and demography of organisms in drylands have drawn much attention recently. However, little is still known about the processes that shaped the species’ spatial genetic structure in areas such as the arid Central Asia, particularly for animals in Northwest China. Here, we investigated the genetic structure and population dynamics of the Zaisan toad-headed agama (Phrynocephalus melanurus) by combining mtDNA phylogeography and species distribution models (SDMs) with range-wide sampling for the first time. Phylogenetic analyses recovered two main Clades, with one from Dzungar and Alakol basins being geographically sub-structured into several groups. Lineage diversification took place in the Pleistocene, coinciding with the drastic aridification caused by Quaternary climatic transitions and drastic activity of the Tianshan Mountains. Moreover, populations of the Dzungar Basin experienced the past expansion and parapatric divergence contributed by isolation-by-distance. SDMs unveiled the species range dynamics since the late Pleistocene, showing expansion in interglacial, and contraction during last glacial maximum and late Holocene periods. Future distribution projections demonstrated drastic habitat loss, suggesting the significance of conservation effort. Our findings highlight the significance of combining genetic approaches with environmental data when evaluating the effects of Pleistocene climatic oscillations. Abstract The agamid lizard Phrynocephalus melanurus is restricted to Northwest China (Dzungar Basin) and the adjacent Eastern Kazakhstan (Zaisan and Alakol basins). To elucidate the phylogeography of P. melanurus, we obtained the mitochondrial DNA COI segments of 175 sampled lizards from 44 localities across the whole distribution. Phylogenetic analyses revealed two main Clades comprising five geographically structured lineages (I, IIa, IIb1, IIb2, and IIb3) that fit an isolation-by-distance (IBD) model. The divergence from the most recent common ancestor was dated to ~1.87 million years ago (Ma). Demographic analyses demonstrated lineage-specific response to past climate change: stable population for Clade I, Subclade IIb1; past population expansion for IIb3 since 0.18 Ma, respectively. Bayesian phylogeographic diffusion analyses detected initial spreading at the Saur Mount vicinity, approximately 1.8 Ma. Historical species distribution model (SDM) projected expansion of the suitable habitat in the last interglacial and shift and contraction in the last glacial maximum and Holocene epochs. The SDM predicted a drastic reduction in suitable area throughout the range as a response to future climate change. Our findings suggest that the evolution of P. melanurus followed a parapatric divergence with subsequent dispersal and adaptation to cold and dry environments during the Quaternary. Overall, this work improves our understanding of the lineage diversification and population dynamics of P. melanurus, providing further insights into the evolutionary processes that occurred in Northwest China and adjacent Eastern Kazakhstan.