Restoring ancestral microbiome aids beetle adaptation to new diets

Eukaryotic hosts often depend on microbes that enhance their fitness, and such relationships may be relatively easily maintained in a stable environment. What is the fate of these associations under rapid environmental change? For instance, if the host switches to a new diet and/or encounters a different microbial community, how does the host-microbiome relationship change? Are the changes adaptive, and how rapidly do they occur? We addressed these questions with the red flour beetle Tribolium castaneum, a generalist insect pest that both consumes and lives in stored grain flour. We found that beetle fitness is enhanced by flour-acquired microbes in the ancestral habitat (wheat flour), but not in novel suboptimal environments (e.g. corn flour) that have a different resident microbial community. Beetles that disperse to new habitats thus have low fitness and a dramatically altered microbiome. Enriching novel habitats with ancestral (wheat-derived) microbes increased beetle fitness, suggesting a viable adaptive strategy. Indeed, within a few generations of laboratory adaptation to two distinct novel habitats, we found that beetle populations gradually restored their ancestral microbiome. Importantly, evolved populations showed a microbe-dependent increase in fecundity and survival on the new diet. We suggest that such repeated, rapid restoration of host-microbe associations may allow generalists to successfully colonize new habitats and escape extinction despite sudden environmental changes.