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The role of the epigenome in phenotypic plasticity is unclear presently. Here we used a multiomics approach (RNA-seq, ChIP-seq, ATAC-seq and Hi-C) to explore the nature of the epigenome in developing honeybee (Apis mellifera) workers and queens. Our data showed that the distinct queen and worker epigenomic landscapes form during the developmental process. Differences in gene expression between workers and queens precede other epigenomic modifications, but the epigenomic differences between workers and queens become more extensive and more layered during development. Genes known to be important for caste differentiation were more likely to be multiply differentially regulated by more than one epigenomic system than other differentially expressed genes. This indicates a multidimensional regulation of expression of key genes, presumably to canalise differences in gene expression. Our data indicate that the epigenome interacts with diverging developmental trajectories rather than controlling them since different epigenomic landscapes form in concert with different developmental outcomes.

Whether a female honey bee (Apis mellifera) develops into a worker or a queen depends on her nutrition during development, which changes the epigenome to alter the developmental trajectory. Beekeepers typically exploit this developmental plasticity to produce queen bee by transplanting worker larvae into queen cells to be reared as queens, thus redirecting a worker developmental pathway to a queen developmental pathway. We studied the consequences of this manipulation for the queen phenotype and methylome over four generations. Queens reared from worker larvae consistently had fewer ovarioles than queens reared from eggs. Over four generations the methylomes of lines of queens reared from eggs and worker larvae diverged, accumulating increasing differences in exons of genes related to caste differentiation, growth and immunity. We discuss the consequences of these cryptic changes to the honey bee epigenome for the health and viability of honey bee stocks.