Taste and pheromonal inputs govern the regulation of time investment for mating by sexual experience in male Drosophila melanogaster

Abstract

Males have finite resources to spend on reproduction. Thus, males rely on a 'time investment strategy' to maximize their reproductive success. For example, male Drosophila melanogaster extends their mating duration when surrounded by conditions enriched with rivals. Here we report a different form of behavioral plasticity whereby male fruit flies exhibit a shortened duration of mating when they are sexually experienced; we refer to this plasticity as 'shorter-mating-duration (SMD)'. SMD is a plastic behavior and requires sexually dimorphic taste neurons. We identified several neurons in the male foreleg and midleg that express specific sugar and pheromone receptors. Using a cost-benefit model and behavioral experiments, we further show that SMD behavior exhibits adaptive behavioral plasticity in male flies. Thus, our study delineates the molecular and cellular basis of the sensory inputs required for SMD; this represents a plastic interval timing behavior that could serve as a model system to study how multisensory inputs converge to modify interval timing behavior for improved adaptation. Author summaryTo maximize their return on investment, male flies utilize a wide variety of sensory inputs, including memories of past sexual encounters. Therefore, when males have sufficient sexual experiences, they shorten their mating duration. The term "Shorter-Mating-Duration" (SMD) was coined to describe this behavior. SMD must be triggered by sugar and pheromone, which is detected by cells and receptors in the male forelegs. We found that these cells include male-specific sensory neurons that are tuned to collect on a male's sexual experiences and relay that information to the brain, where it is used to determine how long to spend mating the next available mate. We hypothesize that SMD can serve as a straightforward genetic model system through which we can investigate "interval timing," the capacity of animals to distinguish between periods ranging from minutes to hours in duration.