The influence of the social environment on the brain circadian transcriptome of two bees differing in the complexity of their society

Social insects provide an attractive model system for studying natural socially-regulated plasticity in circadian rhythms. We compared two highly social bee species differing in their social complexity. The honey bee Apis mellifera has perennial colonies containing tens of thousands of individuals, whereas colonies of the bumble bee Bombus terrestris are annual and contain up to few hundred individuals. We combined behavioral observations and time-series brain RNA sequencing to study the influence of the colony environment and brood tending on circadian gene expression. We sampled bees experiencing four different social environments: Foragers (colony, no brood care), nurses (colony + brood care), individually isolated ("solitary") worker bees (no colony or brood care), and solitary bees with brood (brood care, no colony environment). We analyzed gene expression data using circadian analyses, multivariate analysis, WGCNA, and enrichment analyses. In both species, the circadian expression of the canonical "clock genes" was consistent with previous studies, validating our experimental design and RNA sequencing procedures. As expected, in both species we found the highest number of circadian-regulated genes in behaviorally rhythmic foragers and the lowest in nurses that care for the brood around the clock. Surprisingly however, the solitary with brood group had the second highest number of cycling genes, suggesting that colony factors other than the brood have strong influence on circadian processes in the brain. We will discuss genes and pathways that are circadianly-regulated by the colony environment and brood care, and the implications of these findings to colony social organization.