Reversible switching between epigenetic states in honeybee behavioral subcastes

Female Apis mellifera provide a model of social organization and behavior, with developmental separation of castes into reproductive queens and workers, the latter of which emerge as nurses caring for the brood, and then often shifting behavior to become foragers which gather pollen and nectar outside the hive. Epigenetics, or non-sequence based information heritable during cell division, is an attractive potential substrate for these caste differences and behavioral changes, and we tested the hypothesis that differential DNA methylation might distinguish the brains of queens from workers, or foragers from nurses. Using CHARM microarray analysis and whole genome bisulfite sequencing, we found no evidence of worker-queen differences, but substantial changes were detected in the brains of foragers compared to nurses, in genes involved in chromatin remodeling and RNA processing. To test the link between these changes and worker subcaste phenotypes, we reverted foragers to nurses by a technique of hive trickery. Half of these reprogrammed loci were among the nurse-to-forager subset (P- value < 2.2 x 10-16), and included genes for nuclear transport and organization. These data provide the first evidence of reversible epigenetic changes associated with behavior in a model organism.