Multisensory inputs control 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 novel 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, pheromone and mechanosensory 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.

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

“…Using both theoretical and empirical approaches, we further showed that SMD represents the adaptive behavioral plasticity of male flies (Fig 11). Previous research by our group and others demonstrated that past exposure to rivals lengthens mating duration, a characteristic known as longer-mating-duration (LMD) [14][15][16][17][18][19][20][21][22][23]76]. The two behavioral circuits for LMD and SMD might have evolved independently since they use different sensory cues for detecting 'rivals' or 'females' for 'sexual competition' or 'mating investment', respectively.…”

Long-range neuropeptide relay as a central-peripheral communication mechanism for the context-dependent modulation of interval timing behaviors

“…This behavior is believed to be an adaptation that allows male flies to conserve energy by mating quickly then continuing to other activities (Supplementary information, Fig. S1B) [45][46][47][48] .…”

Peptidergic neurons with extensive branching orchestrate the internal states and energy balance of maleDrosophila melanogaster

“…TRIC serves as a valuable complement to functional Ca 2+ imaging by integrating long-term changes in neuronal activity and providing genetic access to neurons based on their activity. Given that both LMD and SMD require at least 6-12 hours of social isolation or sexual interaction 71,72 , repeated sensory inputs could potentially lead to the accumulation of the modified transcription factor within the nucleus of activated neurons in vivo . Indeed, social isolation or sexual experiences affected the neural activity of GAL4 SIFa-PT -labeled neurons (Fig.…”