Phylogeography and Ecological Niche Modeling of the Alashan Pit Viper (Gloydius cognatus; Reptilia, Viperidae) in Northwest China and Adjacent Areas

Northwest China is characterized by unique geological and historical dynamics and endemic biota, but the joint influence of geography and past climate changes on the evolutionary history of endemic animals is poorly understood. We used two mtDNA genes (ND4 and Cytb) and ecological niche modeling (ENM) to explore how the Quaternary climatic fluctuations and complex geography in Northwest China have shaped genetic diversity, genetic structure, and demographic history of the Alashan pit viper (Gloydius cognatus). Our results clearly show that the lineage diversification of G. cognatus is related to the expansions of deserts and/or the early Pleistocene integration of the Yellow River. The strong spatial genetic structure fits an isolation-by-distance model. The signature of demographic and range contractions during the last glacial maximum (LGM) is rejected by both mitochondrial evidence and ENM. In addition, the suitable habitat of G. cognatus is predicted to be decreased in the future, suggesting that conservation and management of evolutionary significant units (ESUs) should be a priority. Our findings provide the first insights on the evolutionary history of G. cognatus in arid Northwest China and adjacent areas throughout the Quaternary. The joint impacts of historical geological events and Quaternary climatic oscillations in Northwest China on species evolution have been examined extensively in plant under a phylogeographic perspective. However, animal phylogeographic analyses in this region are still limited. The Alashan pit viper, Gloydius cognatus, occurs primarily in arid Northwest China and adjacent areas. Based on variation at two mtDNA genes (ND4 and Cytb) in 27 individuals representing 24 populations, the spatial genetic structure and demographic history of G. cognatus were examined across its geographic range. Phylogenetic analyses revealed two well-supported allopatric clades (each with two distinct subclades/lineages), distributed across the southern (Qaidam Basin, Lanzhou Basin, and Zoige Basin [S1]; Loess Plateau [S2]) and northern (Ily Basin [N1]; Junggar Basin and Mongolian Plateau [N2]) regions. AMOVA analysis demonstrated that over 76% of the observed genetic variation was related to these lineage splits, indicating substantial genetic differentiation among the four lineages. A strong pattern of isolation-by-distance across the sampling populations suggested that geographic distance principally shaped the genetic structure. The four lineages diverged by 0.9-2.2% for the concatenated data, which were estimated to have coalesced similar to 1.17 million years ago (Mya), suggesting that the expansions of the Badain Jaran, Tengger, and Mu Us deserts during the Xixiabangma glaciation likely interrupted gene flow and triggered the observed divergence in the southern and northern regions. Subsequently, the early Pleistocene integration of the Yellow River and associated deserts expansion promoted the differentiation of S1 and S2 lineages (similar to 0.9 Mya). Both mitochondrial evidence and ecological niche modeling (ENM) reject the signature of demographic and range contractions during the LGM for G. cognatus. In addition, ENM predicts that the suitable habitat of G. cognatus will contract in the future. As such, the conservation and management of ESUs should be a priority. Our findings provide the first insights on the lineage diversification and population dynamics of the Alashan pit viper in relation to geological history and Pleistocene climatic oscillations in arid Northwest China.