Carpenter Bees (Xylocopa) Harbor a Distinctive Gut Microbiome Related to That of Honey Bees and Bumble Bees.

Abstract

Eusocial corbiculate bees, including bumble bees and honey bees, maintain a socially transmitted core gut microbiome that contributes to digestion and pathogen defense. In contrast, solitary bees, which have fewer opportunities for direct interhost transmission, typically have less consistent microbiomes dominated by bacteria associated with pollen and food reserves. Carpenter bees (genus Xylocopa) are long-lived bees that are not eusocial but that often live in shared nesting sites. We characterized gut microbiomes for Xylocopa micans, X. mexicanorum, X. tabaniformis parkinsoniae, and X. virginica and for five solitary bee species from other genera (Andrena, Habropoda, Megachile, and Svastra), sampled in the same localities in central Texas. Unexpectedly, all four Xylocopa species had microbiomes dominated by bacterial lineages previously known only from social bees or other insect groups. Microbiomes were similar across three Xylocopa species and included lineages in the families Bifidobacteriaceae, Orbaceae, Lactobacillaceae, Pseudomonadaceae, and Enterobacteriaceae. In contrast, X. virginica had a distinct microbiome dominated by the genus Bombilactobacillus, a group abundant in guts of eusocial bees. Phylogenetic analyses support a past transfer of bacterial lineages into Xylocopa from bumble bees or honey bees. Gut microbiome compositions of Xylocopa species were distinct from those of other co-occurring solitary bees that had variable gut microbiomes dominated by bacteria from environmental sources. IMPORTANCE Gut microbiomes from social bees, such as honey bees and bumble bees, are conserved and consist of host-restricted bacteria that are transmitted among sterile female workers within a colony and that are important to the health of these key insect pollinators. In contrast, solitary bee species typically have more erratic, environmentally acquired microbiomes. Carpenter bees (genus Xylocopa) can be solitary as they lack a worker caste, and each female can excavate nests and raise offspring alone, although females are often social share nests at least in some species. This study showed that the gut microbiomes of four Xylocopa species have distinctive and consistent compositions and are dominated by bacterial lineages previously known from honey bees and bumble bees. Thus, eusociality is not required for bees to maintain a specialized, host-restricted gut microbiome. These findings suggest that gut bacteria are transmitted at shared nesting sites and that they play a role in host ecology.