Sex-specific molecular specialization and activity rhythm-dependent gene expression in honey bee antennae

Abstract

We performed an RNA-seq-based comparison of gene expression levels in the antennae of honey bee drones and time-trained foragers (workers) collected at different times of the day and different activity states. Interestingly, olfaction-related genes [i.e. odorant receptor (Or) genes, odorant binding protein (Obp) genes, carboxyl esterase (CEst) genes, etc.] showed stable gene expression differences between drone and worker antennae. Drone antennae showed higher expression of 24 Or genes, of which 21 belong to the clade X which comprises the receptor for the major queen pheromone compound 9-ODA. This high number of drone-biased Or genes suggests that more than previously thought play a role in sex-pheromone communication. In addition, we found higher expression levels for many non-olfaction-related genes including nitric oxide synthase (NOS), and the potassium channel Shaw. In contrast, workers showed higher expression of 67 Or genes, which belong to different Or clades that are involved in pheromone communication as well as the perception of cuticular hydrocarbons and floral scents. Further, drone antennae showed higher expression of genes involved in energy metabolism, whereas worker antennae showed higher expression of genes involved in neuronal communication, consistent with earlier reports on peripheral olfactory plasticity. Finally, drones that perform mating flight in the afternoon (innate) and foragers that are trained to forage in the afternoon (adapted) showed similar daily changes in the expression of two major clock genes, period and cryptochrome2. Most of the other genes showing hanges with time or onset of daily flight activity were specific to drones and foragers.