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

Abstract

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 wildlife remain unclear. We addressed these questions by monitoring gut microbiomes of wild bumble bees in Southern California, focusing on Bombus vosnesenskii, a major pollinator in western North America. More than a third of all B. vosnesenskii bees exhibited dysbiosis, 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 pathogen infection--all common hallmarks of dysbiosis in other hosts. Other co-occurring Bombus, including two at-risk species, also exhibited dysbiosis. In B. vosnesenskii, dysbiosis was not correlated with certain stressors, such as heat or resource limitation, although other, unmeasured stressors cannot be ruled out. We next examined how dysbiosis varied over two years of sampling. In the first year, dysbiosis emerged only late in the season, when bumble bee colonies normally reproduce and then senesce. Two years later, following an intervening year with historic rainfall and elevated resources, dysbiosis was entrenched throughout the season. These findings show that dysbiosis is both pervasive and highly dynamic in wild bumble bees. The dynamics coincide with host life cycle transitions and environmental change, but the underlying causality remains uncertain. Given that dysbiosis may harm host health, we argue that long-term microbiome monitoring should be considered both for bumble bees and for other wildlife of conservation concern.