The dual coding of a single sex pheromone receptor in regulating the mating behavior of Asian HoneybeeApis cerana

Abstract

AbstractIn honeybee society, a virgin queen usually mates only once with several drones before founding a colony. For the rest of her prolific life, she will not engage in subsequent mating events. In the Asian honeybeeApis cerana, the mechanisms controlling this reproductive strategy involves the queen-released mandibular pheromone (QMP). This pheromone blend regulates the physiology and reproductive behavior of workers and drones. Its main component, 9-oxo-(E)-2-decenoic acid (9-ODA), acts as a sex pheromone and attracts drones. However, how the QMP prevents additional mating later in the queen’s life remains elusive. Using behavioral and chemical analysis, we show that the QMP component methylp-hydroxybenzoate (HOB) released by mated queens inhibits male attraction to 9-ODA. Furthermore,in vivoelectroantennogram and single sensillum recording data indicated that HOB alone significantly reduces the spontaneous spike activity of 9-ODA-sensitive olfactory receptor neurons (ORNs). To explore the molecular mechanism underlying this inverse effect, we conducted qPCR and in situ hybridization assays. The results indicated thatAcerOr11is specifically expressed in sensilla placodea from the drone’s antennae, which are the sensilla that narrowly respond to both 9-ODA and HOB. We then cloned and expressedAcerOr11in a Xenopus oocyte expression system, whereAcerOr11induced robust inward (regular) currents in response to 9-ODA. Intriguingly, HOB induced inverse currents in a dose-dependent manner. This suggests that HOB may act as an inverse agonist againstAcerOr11, providing additional odor-coding information. Based on these findings, we propose a model in whichAcerOr11function as a dual modulators in regulating the mating behavior ofA. cerana. The inverse agonist, HOB, can help manage the population dynamics of honeybees in apiculture.