Gut microbiome mediates an evolutionarily conserved social behavior in eusocial insects

Abstract The gut microbiome is increasingly recognized as a key mediator of social behavior and division of labor in eusocial insects. In some species, trophallactic interactions facilitate nutrient exchange between larvae and adults, creating social interdependency. However, the role of gut bacterial symbionts in this process remains unclear. Here, we investigated the relative contributions of host identity, environment, and trophallactic interactions to gut microbiome assembly in two social wasp species, Vespa orientalis and Vespula germanica, using a cross-fostering, common garden experiment. Newly emerged workers and early-instar larvae were reciprocally exchanged and reared under controlled conditions. High-throughput 16S rRNA gene sequencing and functional inference revealed limited variation across treatments in worker gut communities, mainly shaped by shared environment, indicating stability and environmental dominance. Conversely, larval gut microbiomes were highly plastic, influenced by both larval species and the identity of their nursing workers, highlighting the impact of social interactions. Functional profiles reflected caste-specific roles: workers harbored microbiomes enriched for antimicrobial and detoxification pathways, while larvae microbiomes were enriched in metabolic functions for protein digestion and development. These findings demonstrate that metabolic division of labor in eusocial wasps is supported by life stage-specific microbial communities and functions and maintained by social interactions, positioning the gut microbiome as a key contributor to the maintenance of eusociality.