Multiple pathways mediate the sex-peptide-regulated switch in female Drosophila reproductive behaviours

Male-derived sex-peptide (SP) induces profound changes in the behavior of Drosophila females resulting in decreased receptivity to further mating and increased egg laying. SP can mediate the switch in female reproductive behaviors via a G-protein coupled receptor, SPR, in neurons expressing fruitless, doublesex and pickpocket. Whether SPR is the sole receptor and whether SP induces the post-mating switch in a single pathway has not been tested. Here we report, that the SP response can be induced in the absence of SPR when SP is ectopically expressed in neurons, or when SP, transferred by mating, can access neurons through a leaky blood brain barrier. Membrane-tethered SP can induce oviposition via doublesex, but not fruitless and pickpocket neurons in SPR mutant females. Although pickpocket and doublesex neurons rely on G(ο) signaling to reduce receptivity and induce oviposition, G(ο) signaling in fruitless neurons is only required to induce oviposition, but not to reduce receptivity. Our results show that SP’s action in reducing receptivity and inducing oviposition can be separated in fruitless and doublesex neurons. Hence, the SP induced post-mating switch incorporates shared, but also distinct circuitry of fruitless, doublesex and pickpocket neurons and additional receptors.