Habitat quality influences gut microbiota via cortisol in Siberian flying squirrels ( Pteromys volans)

Interactions between the mammalian neuroendocrine system and the gut microbiota (i.e., the gut-brain axis) can shape how animals cope with environmental challenges. For example, both immune function and the extraction of energy from dietary items depend on microbiota, which can be influenced by the environment directly through transmission or indirectly through neuroendocrine responses. Environmental variation has been shown to translate into variation in microbiome profiles among wild animals, but whether this is due to different environmental microbial transmission or environmental conditions evoking microbiome-modulating physiological stress responses is not known. Here, we investigate covariation among habitat quality, cortisol levels and gut microbiota in adult and juvenile Siberian flying squirrels ( Pteromys volans ) inhabiting a region impacted by variable rates of human disturbance. We test competing hypotheses related to direct (e.g., via diet or transmission) versus indirect (e.g., via the gut-brain axis) effects of habitat on the gut microbiota. Overall, we found that adults had richer gut microbiota and higher concentrations of hair cortisol than juveniles. Our measures of habitat quality exerted direct effects on cortisol concentrations, but had no direct effects on microbiota. Regardless, cortisol predicted microbiota composition among adult squirrels. Finally, structural equation modeling revealed indirect effects of habitat quality on microbial diversity by way of elevations in cortisol among adults. In contrast, among juveniles, habitat-related cortisol variation had no downstream effects on microbial diversity. Together, these findings provide evidence for indirect effects of environmental quality on gut microbiota via the host endocrine system, and suggest these effects can be age-dependent.