The relative importance of genetic distance and adult environment on the worker-worker similarity of gut bacterial microbiome and cuticular hydrocarbon profile in a sweat

The cuticular hydrocarbon profile (CHC profile) and the gut microbiome are two crucial traits that shape the life of bees. The first plays an important role in inter- and intra-specific communication and the latter is essential for the development, nutrition and functioning of the immune system. In honeybees, CHC profile and gut microbiome finely interact: the chemical recognition cues are indeed partially defined by the characteristics of the gut microbiome shared, especially through trophallaxis, among sisters. However, most of the known eusocial bees show more primitive social traits, including moderate genetic relatedness among members of the colony often due to nest drifting or dispersal of workers, and lack of trophallaxis. Hence, primitively eusocial bees offer a great opportunity to evaluate the respective role of worker-worker genetic relatedness and of the environment in which the adult lives (residency nest) on the interaction between CHC profile and gut microbiome. Here, we investigated such relationships in the primitively eusocial digger bee Halictus scabiosae (Halictidae) by analyzing workers from 18 colonies across two Mediterranean nesting sites. We found a high rate of nest-drifting by workers, which leads to a consequent highly variable intra-colonial genetic relatedness. Despite often living in different, often distant nests as adults, workers which were genetically closer (including sisters raised in the same nest) possessed a more similar microbiome profile, but not a more similar CHC profile. Nest residency, indeed, was more correlated with CHC profile than with GM. Distances in microbiome profile and in CHC profile were correlated across workers, but even less of CHC is explained by genetic distance when the autocorrelation of GM is corrected for. Our results point towards an important influence of genetic distance on the gut microbiome, but not on the CHC profile, which is likely to be acquired from nestmates and nest material (i.e. adult environment). This ultimately resulted in a lack of genetic effect on the interaction between these two traits in this primitively eusocial bee.