The gut microbiome of honey-producing wasps has converged on that of social bees

Abstract

Honey-feeding social bees, including honey bees, bumbles bees, and stingless bees, possess distinctive gut bacterial communities that provide benefits to hosts, such as defense against pathogens and parasites. Members of these communities are transmitted through social interactions within colonies. The Mexican honey wasp (Brachygastra mellifica) represents an independent origin of honey-storing within a group of social Hymenoptera. Honey wasps feed on and store honey, but, unlike bees, they prey on other insects as a protein source, and do not consume pollen. We surveyed the gut bacterial communities of Mexican honey wasps across sites within Texas using 16S rRNA profiling, and we estimated bacterial titer per bee using qPCR. For comparison, we also surveyed non-honey feeding wasps from six families, collected in the same region. We found that honey wasp communities are dominated by characteristic bacterial species. In contrast, other wasps had lower absolute titers and more variable communities, dominated by environmental bacteria. Honey wasps from all sampled nests contained strains of Bifidobacterium and Bombilactobacillus that were closely related to symbionts of bumble bees and other bees, suggesting acquisition via host-switching. Some individuals also harbored a close relative of Candidatus Schmidhempelia bombi (Orbaceae), an uncultured bumble bee symbiont, again suggesting host-switching. The most prevalent species was an uncultured Lactobacillus that potentially represents an independent acquisition of environmental Lactobacillus. The transition to honey feeding, combined with a highly social life history, appears to have facilitated the establishment of a bacterial community with similarities to those of social bees. IMPORTANCEHoney-feeding social insects such as honey bees and bumble bees have conserved gut bacterial communities that are transmitted among nestmates. These bacteria benefit hosts by providing defense against pathogens, and potentially by contributing to pollen digestion. The bacterial communities of wasps are less studied. Whereas most wasps are carnivorous and consume nectar, honey wasps (Brachygastra spp.) store and eat honey. Here, we address the consequences of this dietary shift for the gut community. Using field collections of Mexican honey wasps and other co-occurring wasps, we found that honey wasps have distinctive gut bacterial communities. These include several bacteria most closely related to bacteria in bumble bees, suggesting their acquisition via host-switching. Solitary wasps and social wasps that do not make honey have smaller gut communities dominated by environmental bacteria, suggesting that honey feeding has shaped the gut bacterial communities of honey wasps.