The gut microbiome facilitates ecological adaptation in an invasive vertebrate

ABSTRACT Gut microbial communities regulate host physiology and health of humans and laboratory animals. The functional significance of these collective bacterial genomes (i.e. the microbiome) to the adaptive potential of wildlife hosts is still unknown. Studies demonstrating convincing examples of microbial flexibility to environmental change so far lack the experimental approaches to demonstrate the effect on host physiology. Invasive species provide natural experiments to tease apart these host-microbe relationships. However, no studies have investigated how microbial symbionts might mediate responses of invasive hosts’ physiology to environmental change. In this study, we examine whether invasive gut microbiomes have significantly diverged in their ability to respond to novel environmental change (i.e. a dietary challenge) compared to native gut microbiomes by performing reciprocal faecal microbial transplant (FMT) experiments in native and invasive guttural toad ( Sclerophrys gutturalis ) populations. Subsequently, we determine how the microbiome regulates host physiological changes in response to a dietary challenge. We show that invasive gut microbiomes exhibit higher microbial compositional and predicted functional flexibility to novel dietary change, compared to native gut microbiomes. This increased microbial flexibility is coupled with significant flexibility in energy harvesting. Furthermore, our results indicate that overall invasive gut microbiomes significantly upregulate energy harvesting and physiological performance of hosts, compared to native microbiomes. Our study is the first identifying gut microbiota as the sole factor contributing to the adaptive physiology of a vertebrate using a unique study design. These findings provide novel insights into the key role of gut microbial symbionts in increasing the invasive potential of its vertebrate host.