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

Abstract

ABSTRACTHoney-feeding social bees, including honey bees and bumble bees, possess distinctive gut microbiomes that provide benefits to hosts, such as defense against pathogens and parasites. Microbiome members 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 they prey on other insects as a protein source, and do not consume pollen as do bees. We surveyed the gut microbiomes of Mexican honey wasps across sites within Texas using 16S rRNA community profiling, and we estimated microbiome size using qPCR. For comparison, we also surveyed non-honey feeding wasps from six families, collected in the same region. We found that honey wasps have large microbiomes dominated by characteristic bacterial species, in contrast to other wasps, which had smaller, more variable microbiomes dominated by environmental bacteria. All honey wasps contained strains ofBifidobacteriumandBombilactobacillusthat were closely related to symbionts of bumble bees and other bees, suggesting their acquisition via host-switching. Some individuals also harbored a close relative ofCandidatusSchmidhempelia bombi (Orbaceae), an uncultured bumble bee symbiont, again suggesting host-switching. The most prevalent species was an unculturedLactobacillus, related toL. acetotolerans, and potentially representing an independent acquisition of environmentalLactobacillus. The switch to honey feeding, combined with a highly social life history, appears to have facilitated the establishment of a microbiome resembling those of honey bee and bumble bees.IMPORTANCEHoney-feeding social insects such as honey bees and bumble bees have conserved gut microbiomes that are transmitted among nestmates. The bacteria consist of host-associated species that benefit the bee hosts by providing defense against pathogens and parasites, and potentially by contributing to digestion. The microbiomes of wasps are less studied, although some species have bacteria found in solitary bees. Here, we looked at a group of wasps that have a diet much like that of honey bees, predicting that a diet switch from nectar to stored honey available year-round enabled them to acquire a microbiome like that of honey-feeding bees. Honey wasps (Brachygastraspp.) are the only group of wasps that store honey. Their large nests are made from paper, and colonies survive for several years. We found that Mexican honey wasps have a conserved gut microbiome with similarities to those of other honey-feeding bees. Several microbiome members are most closely related to bacteria in bumble bees, suggesting their acquisition via host switching. The most common member was a previously unknownLactobacillus. Solitary wasps and other paper wasps that do not make honey have smaller microbiomes dominated by environmental bacteria, suggesting that honey feeding has shaped the gut bacterial communities of honey wasps.