Nutrients And Pheromones Promote Insulin Release To Inhibit Courtship Drive In Drosophila

Food and reproduction are the two fundamental needs for all animals.However,under fluctuating living environments in nature,animals often have to choose between feeding and reproduction to maintain the balance between survival and reproduction.Since sexual activities are energy-consuming,male animals must prevent futile courtship to save energy.Feeding can replenish energy,so there must be a balance between feeding and reproduction to maintain energy homeostasis in animals.However,the neural mechanisms that orchestrate nutrient intake and sexual behaviors are not well understood.Here,we combined genetic and behavioral approaches to investigate courtship behaviors of male Drosophila under different conditions.Firstly,we found that sugar feeding could make IPCs in the brain release DILP2 and suppress the mating drive of male flies to virgin flies.Secondly,we proved that activating IPCs could inhibit courtship-promoting P1 neurons through insulin receptors,and male flies with mutation of dilp2 exhibited an elevated courtship index toward unreceptive mates,including males,mated females and virgin females from other species.Thirdly,we found that aversive pheromones could also make male flies release DILP2,which is mediated by CCAP through screening.By optogenetically activating ppk23 neurons which can detect aversive pheromones and be co-labelled with CCAP,we proved the activation of ppk23 neurons could release CCAP,which acted on CCAP receptors on IPCs to trigger DILPs release.Lastly,we observed there was a delayed onset of futile courtship when any component of CCAP-DILP2-P1 signaling was disrupted.Combined with previous studies,we found that ppk23 neurons could not only relay the information to P1 neurons via neuronal connections but also via a neuropeptidergic pathway.In summary,we identified a neuropeptidergic neural circuit underlying mating decision,and revealed a direct link between “metabolic center” IPCs and “sex center”P1 neurons in Drosophila melanogaster.In addition,CCAP-DILP2-P1 signaling mediated a delayed inhibition while ppk23-m AL-P1 pathway could rapidly suppress male’s sexual drive to futile mates(Kallman et al.,2015).We demonstrated an elegant strategy used by the nervous system to fine-tune central neurons’ activity during courtship behaviors,which elucidates for the first time that the same group of peripheral sensory neurons can mediate similar physiological functions through both fast and slow pathways.Besides,given the highly conserved insulin signaling across different species,our study provides a reference for the relationship between feeding and reproduction in mammals.