The gut microbiome defines social group membership in honey bee colonies

In the honey bee, genetically related colony members innately develop colony-specific cuticular hydrocarbon profiles, which serve as pheromonal nestmate recognition cues. Yet, despite high intracolony relatedness, the innate development of colony-specific chemical signatures by individual colony members is largely determined by the colony environment, rather than solely relying on genetic variants shared by nestmates. Therefore, it is puzzling how a nongenic factor could drive the innate development of a quantitative trait that is shared by members of the same colony. Here, we provide one solution to this conundrum by showing that nestmate recognition cues in honey bees are defined, at least in part, by shared characteristics of the gut microbiome across individual colony members. These results illustrate the importance of host-microbiome interactions as a source of variation in animal behavioral traits.

Chemical signatures of honey bee group membership develop via a socially-modulated innate process

Large social insect colonies exhibit a remarkable ability for recognizing group members via colony-specific cuticular hydrocarbon (CHC) pheromonal signatures. Previous work suggested that in some ant species colony-specific signatures are generated through a “gestalt” mechanism via the passive transfer and homogenization of CHCs across all individual members of the colony. In contrast, we demonstrate that nestmate recognition cues of worker honey bees (Apis mellifera) mature in foragers via a sequence of stereotypic age-dependent quantitative and qualitative chemical transitions, which are driven by intrinsic biosynthetic pathways. Therefore, in contrast to predictions of the “Gestalt” model, nestmate recognition cues in honey bee colonies do not represent a passive “average” signature that is carried and recognized by all colony members. Instead, specific colony members develop the relevant cues via an innately-determined developmental program that can be modulated by colony-specific social environmental factors.

Increased genetic diversity as a defence against parasites is undermined by social parasites: Microdon mutabilis hoverflies infesting Formica lemani ant colonies

Genetic diversity can benefit social insects by providing variability in immune defences against parasites and pathogens. However, social parasites of ants infest colonies and not individuals, and for them a different relationship between genetic diversity and resistance may exist. Here, we investigate the genetic variation, assessed using up to 12 microsatellite loci, of workers in 91 Formica lemani colonies in relation to their infestation by the specialist social parasite Microdon mutabilis . At the main study site, workers in infested colonies exhibited lower relatedness and higher estimated queen numbers, on average, than uninfested ones. Additionally, estimated queen numbers were negatively correlated with estimated average numbers of mates per queen within infested colonies. At another site, infested colonies also exhibited significantly lower worker relatedness, and estimated queen numbers were comparable in trend. In contrast, in two populations of F. lemani where M. mutabilis was absent, relatedness within colonies was high (40 and 90% with R >0.6). While high genetic variation can benefit social insects by increasing their resistance to pathogens, there may be a cost in the increased likelihood of infiltration by social parasites owing to greater variation in nestmate recognition cues. This study provides the first empirical test of this hypothesis.