Pervasive and dynamic gut dysbiosis in wild bumble bees is linked to the host life cycle

Stressors can shift the microbiome into an altered, "dysbiotic" state that reduces host fitness. While well-studied in humans and laboratory models, the prevalence, predictability, and drivers of dysbiosis in nature remain unclear. We addressed these questions by monitoring gut microbiomes of a wild bumble bee (Bombus vosnesenskii) population in Southern California. We found that dysbiosis is highly pervasive: more than a third of all bees were dysbiotic, when defined as a >50% replacement of host-specialized core bacteria by environmental bacteria. This replacement covaried with increased alpha and beta diversity, an enrichment of oxygen-tolerant taxa, and pathogens--all common hallmarks of dysbiosis in other hosts. Given that dysbiosis may be harmful, and that bumble bees are in decline globally, there is a clear need for monitoring and experiments to determine if dysbiosis elevates bumble bee extinction risk. Surprisingly, dysbiosis was not associated with a morphological indicator of stress nor with a variety of potential stressors. It instead appears to be intrinsic to the host life cycle. In the first year of sampling, dysbiosis emerged only late in the season, when bumble bee colonies normally reproduce and then senesce. But following historic rainfall and a sustained resource base, B. vosnesenskii life history shifted, and dysbiosis was entrenched throughout the season. These findings show how dysbiosis may be regulated by the host life cycle, yet also change unpredictably due to life history plasticity. As the climate becomes more extreme and erratic, so too may host life cycles and microbiome dynamics, with uncertain consequences.