Evolutionary history of multiple mountain ungulates reveals refugia and population expansion in response to Quaternary change in the East Himalaya-Hengduan Mountains

Quaternary geological events, glacial cycles, and climate fluctuations have a profound influence on the evolutionary history and population dynamics of many species. Mountain ungulates offer an ideal model for researching these historical processes. In this study, three taxa of mountain ungulates (Capricornis, Naemorhedus, and Muntiacus), which share overlapping ecological niches and similar life-history strategies, were selected to analyze the impact of historical events on their evolution and population dynamics. Specimens were collected from naturally deceased individuals during multiple field expeditions, as well as from forest police seizures, and included skulls, skins, and dried meat. Mitochondrial genomes (mitogenomes) were used as molecular markers. Analyses indicated that the evolutionary divergence of these mountain ungulates was primarily driven by five major uplift phases of the Qinghai-Xizang Plateau and a series of glaciation events. Results also indicated the formation of multiple refugia in the East Himalaya-Hengduan Mountains (EHHM) during the Quaternary. Four species—Capricornis sumatraensis, Naemorhedus cranbrooki, Naemorhedus evansi, and Muntiacus gongshanensis—were selected for detailed analyses of historical population dynamics. Notably, population expansions were detected for all species, with the expansions of N. cranbrooki, N. evansi, and M. gongshanensis occurring during the early to mid-Holocene, likely due to warmer and more humid climatic conditions. In contrast, the population expansion of C. sumatraensis occurred in the late Holocene, driven by forest retreat and increased human activities such as settlement and grazing. Additionally, and most importantly, we obtained molecular samples of N. cranbrooki in Xizang, China, for the first time, and also confirmed the distribution of N. cranbrooki in Xizang rather than being limited to northern Myanmar. Overall, these findings provide evidence that N. cranbrooki is distributed in Xizang, also offer novel insights into the connections between Quaternary environmental change and species differentiation, refugia formation and population dynamics of mountain ungulates in the EHHM region.