Hormonal Modulation of Pheromone Detection Enhances Male Courtship Success

•Or47b odorant receptor is required for the copulation advantage of older males•Older males display a higher Or47b neuronal sensitivity to pheromones•Age-dependent sensitization of the Or47b neurons is controlled by juvenile hormone•Juvenile hormone targets Or47b ORNs to regulate age-dependent male mating drive

SummaryDuring the lifespans of most animals, reproductive maturity and mating activity are highly coordinated. In Drosophila melanogaster, for instance, male fertility increases with age, and older males are known to have a copulation advantage over young ones. The molecular and neural basis of this age-related disparity in mating behavior is unknown. Here, we show that the Or47b odorant receptor is required for the copulation advantage of older males. Notably, the sensitivity of Or47b neurons to a stimulatory pheromone, palmitoleic acid, is low in young males but high in older ones, which accounts for older males’ higher courtship intensity. Mechanistically, this age-related sensitization of Or47b neurons requires a reproductive hormone, juvenile hormone, as well as its binding protein Methoprene-tolerant in Or47b neurons. Together, our study identifies a direct neural substrate for juvenile hormone that permits coordination of courtship activity with reproductive maturity to maximize male reproductive fitness.