Modulation of sex pheromone detection by nutritional and hormonal signals in a male insect

As in other animals, insects can modulate their odor-guided behaviors, especially sexual behavior, according to environmental and physiological factors such as the individual's nutritional state. This behavioral flexibility results from modifications of the olfactory pathways under the control of hormones. Most studies have focused on the central modulation of the olfactory system and less attention has been paid to the peripheral olfactory system. To understand how nutritional inputs influence the detection of sex pheromones in insects, we turned to the male moth Agrotis ipsilon, for which the behavioral responsiveness to sex pheromones is dependent on diet and reproductive hormones, juvenile hormone (JH) and 20-hydroxyecdysone (20E). We demonstrated that a sugar-rich diet with sodium increases the sensitivity of olfactory receptor neurons to (Z)-7-dodecen-1-yl acetate, the major sex pheromone compound, and the antennal expression of the pheromone binding protein (PBP2) and the pheromone receptor (OR3). Such a diet also induces overexpression of the methoprene-tolerant receptor to JH and underexpression of the ecdysone receptor to 20E in antennae. The diet-induced olfactory responses were maintained by treatment with cucurbitacin B, a 20E antagonist, but were suppressed by the topic application of precocene, a JH biosynthesis inhibitor. These findings reveal that a positive nutritional state enhances sex pheromone detection through JH actions on the peripheral actors of the pheromone system in male moths. More broadly, in insects, our study provides, for the first time, a neuronal and molecular basis of the dietary-dependent endocrine modulation of the peripheral olfactory system.