Temporal and spatial variations in body mass and thermogenic capacity associated with alterations in the gut microbiota and host transcriptome in mammalian herbivores

Abstract

Most wild animals follow Bergmann's rule and grow in body size as cold stress increases. However, the underlying thermogenic strategies and their relationship with the gut microbiota have not been comprehensively elucidated. Herein, we used the plateau pikas as a model to investigate body mass, thermogenic capacity, host transcriptome, gut microbiota and metabolites collected from seven sites ranging from 3100 to 4700 m on the Qinghai–Tibetan Plateau (QTP) in summer and winter to test the seasonal thermogenesis strategy in small herbivorous mammals. The results showed that the increase in pika body mass with altitude followed Bergmann's rule in summer and an inverted parabolic shape was observed in winter. However, physiological parameters and transcriptome profiles indicated that the thermogenic capacity of pikas increased with altitude in summer and decreased with altitude in winter. The abundance of Firmicutes declined, whereas that of Bacteroidetes significantly increased with altitude in summer. Phenylalanine, tyrosine, and proline were enriched in summer, whereas carnitine and succinate were enriched in winter. Spearman's correlation analysis revealed significant positive correlations between Prevotella, Bacteroides, Ruminococcus, Alistipes and Akkermansia and metabolites of amino acids, pika physiological parameters, and transcriptome profiles. Moreover, metabolites of amino acids further showed significant positive correlations with pika physiological parameters and transcriptome profiles. Our study highlights that the changes in body mass and thermogenic capacity with altitude distinctly differentiate small herbivorous mammals between summer and winter on the QTP, and that the gut microbiota may regulate host thermogenesis through its metabolites.