Convergent Evolution of Rumen Microbiomes in High-Altitude Mammals

Abstract

Studies of genetic adaptation, a central focus of evolutionary biology, most often focus on the host's genome and only rarely on its co-evolved microbiome. The Qinghai-Tibetan Plateau (QTP) offers one of the most extreme environments for the survival of human and other mammalian species. Yaks (Bos grunniens) and Tibetan sheep (T-sheep) (Ovis aries) have adaptations for living in this harsh high-altitude environment, where nomadic Tibetan people keep them primarily for food and livelihood [1]. Adaptive evolution affects energy-metabolism-related genes in a way that helps these ruminants live at high altitude [2, 3]. Herein, we report convergent evolution of rumen microbiomes for energy harvesting persistence in two typical high-altitude ruminants, yaks and T-sheep. Both ruminants yield significantly lower levels of methane and higher yields of volatile fatty acids (VFAs) than their low-altitude relatives, cattle (Bos taurus) and ordinary sheep (Ovis aries). Ultra-deep metagenomic sequencing reveals significant enrichment in VFA-yielding pathways of rumen microbial genes in high-altitude ruminants, whereas methanogenesis pathways show enrichment in the cattle metagenome. Analyses of RNA transcriptomes reveal significant upregulation in 36 genes associated with VFA transport and absorption in the ruminal epithelium of high-altitude ruminants. Our study provides novel insights into the contributions of microbiomes to adaptive evolution in mammals and sheds light on the biological control of greenhouse gas emissions from livestock enteric fermentation.

Effect of dietary energy on digestibilities, rumen fermentation, urinary purine derivatives and serum metabolites in Tibetan and small‐tailed Han sheep

“…In the present study, the total VFA concentration was greater in Tibetan than in Han sheep, and, therefore, Tibetan sheep were able to derive more energy than Han sheep from the same feed intake, suggesting a greater degradation of nutrients in the rumen of Tibetan sheep. This was due to, at least in part, the report that rumen microbial genes of Tibetan sheep were richer in VFA‐yielding pathways than Han sheep (Zhang et al, ). The lower rumen pH in Tibetan than in Han sheep was due to the greater VFA accumulation in the rumen (Nikkhah, ).…”

Selection signatures for high‐altitude adaptation in ruminants

“…In a subsequent transcriptome analysis, Zhang et al () showed higher expression in the high‐altitude species compared with their lowland counterparts for genes that are associated with VFA transport and absorption in the ruminal epithelium. Moreover, a metagenomic analysis of the rumen in both Tibetan sheep and yak revealed co‐enrichment in VFA‐yielding pathways of rumen microbial genes, which further indicates a co‐evolution of the microbiome and the host genome in response to altitude adaptation (Zhang et al ).…”

Comparison of the gut microbiota composition between the wild and captive Tibetan wild ass ( Equus kiang )

“…The Qinghai‐Tibetan plateau provides one of the most extreme environments for the survival of humans and other mammals (Zhang et al . ). The Tibetan wild ass ( Equus kiang ) is a unique species on the Qinghai‐Tibetan plateau and is widely distributed in Qinghai, Gansu, Xinjiang, Sichuan and Tibet (Wu and Yi ; Moehlman ).…”