Did the expansion of C4 plants drive extinction and massive range contraction of micromammals? Inferences from food preference and historical biogeography of pikas

Abstract

The expansion of C4 plants is thought to have profound effects on the faunal turnover of large mammals during the latest Miocene. However, it is unclear whether this event also induced extinction and range contraction of small mammals. Pikas (Ochotonidae) are highly adapted to arctic or alpine environments, and are considered ideal indicators in biochronology. Previous studies have demonstrated that large numbers of ochotonides were widely geographically distributed in the middle Miocene, although most went extinct in the late Miocene. It is uncertain whether their extinction was induced by the accelerated expansion of C4 plants. A comprehensive review of the worldwide fossil occurrence in Ochotonidae and a detailed analysis of its historical biogeography are also lacking. Here, we categorize plants that are selected by extant pikas for food and hay piles according to their photosynthesis pathway. Fossil records of Ochotonidae are also reviewed. The divergence time within Ochotona is estimated using multiple fossil calibrators and the combined matrix of two mitochondrial genes. We also infer the historical biogeography of Ochotona using event based methods (S-DIVA, Bayes-DIVA and Maximum Parsimony). The expansion of C4 plants in the late Miocene may have resulted in the extinction and range contraction of pikas. This hypothesis is supported by the prominent preference of C3 plants in extant pikas. The Qinghai–Tibet Plateau is identified as the most likely ancestral center or origin of extant Ochotona. Evolution of the pikas' geographical range shows a strong concordance with the global climate and paleoecological change. Their historical extinction and recent range contraction, as well as future survival prospects, appear to be closely associated with climate-driven vegetation changes in their habitats.