Selection for high metabolic rate reduces gut microbiota responsiveness to dietary restriction in bank voles

Abstract

Host-microbiota interactions are crucial in adapting to environmental changes, such as fluctuating energy availability. Yet, the extent to which hosts and their microbiota exhibit coordinated plasticity in response to transient energy limitation remains unclear. Here, we examined the capacity for parallel reversible plasticity in hosts and gut microbiota to temporary dietary restriction in hosts with differing energy needs. We subjected bank voles (Clethrionomys glareolus) from a long-term artificial selection experiment for high aerobic metabolism (A-lines) and control lines (C-lines) to dietary restriction (food dilution with insoluble fiber) followed by a recovery period. We measured traits relevant for vole energy consumption and fecal microbiota composition at baseline, after dietary restriction, and after recovery. We hypothesized that A-line voles would experience more severe and prolonged physiological effects of dietary restriction than C-line voles, which might be counteracted by higher microbiota responsiveness. Dietary restriction caused a temporary increase in food consumption, decrease in body mass and resting metabolic rate, and significant shifts in gut microbiota composition, all of which returned to near baseline levels during the recovery period. These effects were largely similar for the selection lines, but contrary to our prediction, the effect of dietary restriction on bacterial diversity was stronger in C-lines. This suggests higher resistance of the A-line microbiota to dietary changes, perhaps resulting from increased host control over microbial communities due to the directional selection for high metabolic capacity. Overall, our findings highlight a substantial capacity for reversible plasticity in host physiology and gut microbiota in fluctuating environments.