Epigenetic regulation of caste determination and queen life stage transitions in the buff-tailed bumble bee, Bombus terrestris

Polyphenism in the buff-tailed bumble bee, Bombus terrestris, is an interesting example of developmental plasticity. One genome produces three distinct organisms (two diploid females, the reproductive queen and workers, and haploid male drones). The queen/worker phenotype is thought to be determined by the amount of diet and the pheromone environment during post-embryonic development. Studies in Hymenoptera have demonstrated that chromatin-based epigenetic regulation is a key determinant of the distinct patterns of gene expression that drive caste-specific phenotypic and behavioural differences. Here, from performing CUT&RUN and RNA-seq in brain tissue, I produce the first genome-wide maps of chromatin structure in queen and worker bumble bees, at the end point of developmental plasticity and start of adult behavioural maturation. I find histone post-translational modifications (H3K4me1, H3K4me3, H3K27ac and H3K27me3) in newly emerged queen and worker bumble bees correlate with transcription and find genome-wide differences in H3K27ac between the two female castes. Bumble bee colonies also show remarkable behavioural plasticity during adult maturation, in particular a reproductive division of labour that is central to eusociality, where queens are the only female in the colony to mate. Furthermore, only bumble bee queens enter diapause during winter when temperatures are low and resources scarce. I hypothesised that both mating and diapause, key caste specific events in the queen life cycle, may drive differential gene expression to consolidate the queen phenotype and behaviour. I demonstrate that between diapausing/pre-diapause queens and virgin/mated queens there are extensive differences in chromatin structure and identify key differences in associated transcriptional networks. Taken together, this study provides the first genome wide map of chromatin features in the queen and worker phenotypes of Bombus terrestris, and in two distinct queen behavioural states: after diapause and mating. As a primitively eusocial insect, these findings provide novel data on environmentally driven phenotypic plasticity, caste-specific behaviours and the molecular basis of eusociality