Differences in Gut Microbes Across Age and Sex Linked to Metabolism and Microbial Stability in a Hibernating Mammal

The gut microbiome has a well-documented relationship with host fitness, physiology, and behavior. However, most of what is known comes from captive animals where diets and environments are more homogeneous or controlled. Studies in wild populations that experience dynamic environments and have natural life history variation are less common but are key to understanding the drivers of variation in the gut microbiome. Here we examine a wild population of yellow-bellied marmots (<i>Marmota flaviventer</i>), an obligate winter hibernator, to quantify multivariate associations between host-associated factors (e.g., age, sex, environmental harshness, and social behavior) and gut microbial composition. Across 5 years and 143 individuals, we found that males had a higher relative abundance of microbes associated with mass gain and cellulose digestion, which suggests a metabolic investment in mass gain (such as phylum <i>Firmicutes</i> and family <i>Lachnospiraceae</i>). By contrast, females had higher relative abundances of microbes associated with inflammation and metabolism (from microbial groups such as <i>Tenericutes</i> and <i>Ruminococcus</i>), possibly reflecting the importance of lactation and offspring investment. Post hoc analyses of lactating females showed a negative relationship with the abundance of microbes associated with mass gain but a positive relationship with microbes associated with metabolic energy, suggesting a trade-off between investment in pups and maternal mass gain. Older animals also had reduced <i>Proteobacteria</i> relative abundance, a phylum associated with reduced inflammation. Results demonstrate that sex and age-based traits, not sociality or environmental harshness, are associated with microbe-mediated metabolism and inflammation in a wild, hibernating mammal.