Diet and endocrine effects on behavioral maturation-related gene expression in the pars intercerebralis of the honey bee brain

Nervous and neuroendocrine systems mediate environmental conditions to control a variety of life history traits. Our goal was to provide mechanistic insights as to how neurosecretory signals mediate division of labor in the honey bee (Apis mellifera). Worker division of labor is based on a process of behavioral maturation by individual bees, which involves performing in-hive tasks early in adulthood, then transitioning to foraging for food outside the hive. Social and nutritional cues converge on endocrine factors to regulate behavioral maturation, but whether neurosecretory systems are central to this process is not known. To explore this, we performed transcriptomic profiling of a neurosecretory region of the brain, the pars intercerebralis (PI). We first compared PI transcriptional profiles for bees performing in-hive tasks and bees engaged in foraging. Using these results as a baseline, we then performed manipulative experiments to test whether the PI is responsive to dietary changes and/or changes in juvenile hormone (JH) levels. Results reveal a robust molecular signature of behavioral maturation in the PI, with a subset of gene expression changes consistent with changes elicited by JH treatment. In contrast, dietary changes did not induce transcriptomic changes in the PI consistent with behavioral maturation or JH treatment. Based on these results, we propose a new verbal model of the regulation of division of labor in honey bees in which the relationship between diet and nutritional physiology is attenuated, and in its place is a relationship between social signals and nutritional physiology that is mediated by JH.