Phylogeography and ecological niche modeling unravel the evolutionary history of the Yarkand hare, Lepus yarkandensis (Mammalia: Leporidae), through the Quaternary

Abstract

Background: The Taklimakan Desert in China is characterized by unique geological and historical dynamics and endemic flora and fauna, but the influence of historical climate oscillations on the evolutionary history of endemic animals is poorly understood. Lepus yarkandensis is an oases-dependent Near Threatened species that lives in fragmented oasis habitats in the Taklimakan Desert, China. We investigated the geological and climatic impacts on its geographical differentiation, demographic history and influence of Pleistocene glacial-interglacial cycles on the evolutionary history of L. yarkandensis. Further, studied the impact of climatic oscillation based modification on phylogeography, distribution and diversification pattern of Yarkand hare by using Cytb (1140 bp), MGF (592 bp) and SPTBN1 (619 bp) markers. Ecological niche modeling (ENM) revealed the evolutionary history of this species in response to climate change during the Quaternary. Paleodistribution modeling was used to identify putative refugia and estimate their historical distributions. Results: Both historical demographic analyses and climatic niche modeling revealed strong effects of glacial climate changes, suggesting recurrent range contractions and expansions. The EBSP results indicated clear population expansion of L. yarkandensis since the Pleistocene. In the "early Pleistocene", the demographic expansion continued from 0.83 MYA to the last glacial period. The ENM analysis supported a wide distribution of Lepus yarkandensis at high altitudes during the last interglacial (LIG) period. During the last glacial maximum (LGM), the suitable climate was reduced and restricted to the western part of the Taklimakan Desert. Conclusions: Inland aridification, oasis evolution and river flow played major roles in the population differentiation and demographic history of Yarkand hares. Historically, the large, continuous oases in the Taklimakan Desert contained a viable and unique population of L. yarkandensis. The fragmented desert environment might have caused low gene flow between individuals or groups, thus leading to predominant genetic differentiation. The Pleistocene climatic cycles triggered the diversification and expansion of this species during cold and warm periods, respectively, leading to multiple colonization events within the Taklimakan Desert. These events might be due to the expansion of the Taklimakan Desert during the Middle Pleistocene. Yarkand hare previously occupied vast areas at low and intermediate altitudes in Xinjiang, Gansu, Shanxi, Henan and Shaanxi Provinces in China. The past aridification, climate change-induced oasis modifications, changes in river volumes and flow directions, and human activities all affected the population demography and phylogeography of the Yarkand hare.