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.

Drosophila melanogaster is a suitable model for investigating how neuropeptides influence animal behaviours and physiology. We previously reported that two behavioural paradigms control mating duration of male Drosophila, called Longer-Mating-Duration (LMD) andShorter-Mating-Duration (SMD) that are induced through socio-sexual environment prior to copulation. Understanding the molecular and cellular mechanisms by which males exhibit plasticity to different social cues remains poorly understood. Here, we show that SIFa modulates the neural circuitry for both LMD and SMD. Neuropeptide-to-neuropeptide communication, so called 'neuropeptide relay' plays a key role to mediate this control. We identified that 7 neuropeptides expressed in SIFa Receptor-positive cells are functionally important to regulate either LMD and/or SMD. The modulation of two independent mating duration behaviour by the different SIFa-mediated neuropeptide relay will help to further investigate how the neuropeptidergic modulation can control complex behaviours.

Males have a finite resource for reproduction; they rely on a 'time investment strategy' to maximize reproductive success. Here we report a novel behavioral plasticity whereby male fruit flies exhibit a shortened mating duration when sexually satiated, which we named 'Shorter-Mating-Duration (SMD)'. SMD requires the sexually dimorphic Gr5apositive neurons for detecting female body pheromones, and can be induced by 2 gustatory stimuli. The memory circuitry within the ellipsoid body (EB) and mushroom body (MB) brain regions is crucial for SMD, which depends on the circadian clock genes Clock and cycle, but not timeless or period. SMD also relies on signaling via the neuropeptide sNPF, but not PDF or NPF. Sexual experience modifies the neuronal activity of a subset of sNPF-positive neurons involved in neuropeptide signaling, which modulates SMD. Thus, our study delineates the molecular and cellular basis for SMDa plastic social behavior that serves as a model system to study how the brain switches the internal states between sexual drive and satiety. (Bretman et al., 2011a). Behavioral plasticity requires the formation of association between a proper behavioral output and given information, as the consequences of multiple interactions between evolutionarily programmed innate behaviors and cumulated learning experiences of the animal (Dissel et al., 2015;Lupold et al., 2011).What are the general terms of behavioral plasticity and what is its meaning in the context of the fruit fly's sexual behavior? One example of plastic male behavior is 'Longer-Mating-Duration (LMD)', with increased investment via mating duration lengthening induced by exposure to rivals before mating (Bretman et al., 2009). In Drosophila, males respond to the presence of rivals by prolonging mating duration to guard the female and pass their genes. In previous studies, we examined the genetic network and neural circuits that regulate rival-induced longer mating duration (LMD).LMD can be induced solely via visual stimuli. LMD depends on the circadian clock genes timeless and period, but not Clock or cycle. LMD involves the memory circuit of the ellipsoid body (EB). Further, we identified a small subset of clock neurons in the male brain that regulates LMD via neuropeptide signaling (Kim et al., 2013).Here we report a novel plastic behavior of male D. melanogaster for its selective investment in mating. Sexually satiated Drosophila males show this plastic behavior by limiting their investment in copulation time, namely 'Shorter-Mating-Duration (SMD)'. In addition to delineating the requisite circuitry by identifying the neurons for SMD, our study has uncovered the sensory stimuli, clock genes, sexual dimorphism, and neuropeptide signaling crucial for the SMD behavior, which is functionally and 6 mechanistically distinct from the previously identified LMD pathway.