The neuropeptide sulfakinin is a peripheral regulator of insect behavioral switch between mating and foraging

Behavioral strategies for foraging and reproduction in the oriental fruit fly (Bactrocera dorsalis) are alternative options for resource allocation and are controlled by neuropeptides. Here, we show that the behavioral switch between foraging and reproduction is associated with changes in antennal sensitivity. Starved flies became more sensitive to food odors while suppressing their response to opposite-sex pheromones. The gene encoding sulfakinin receptor 1 (SkR1) was significantly upregulated in the antennae of starved flies, so we tested the behavioral phenotypes of null mutants for the genes encoding the receptor (skr1^-/-) and its ligand sulfakinin (sk^-/-). In both knockout lines, the antennal responses shifted to mating mode even when flies were starved. This suggests that sulfakinin signaling via SkR1 promotes foraging while suppressing mating. Further analysis of the mutant flies revealed that sets of odorant receptor (OR) genes were differentially expressed. Functional characterization of the differentially expressed ORs suggested that sulfakinin directly suppresses the expression of ORs that respond to opposite-sex hormones while enhancing the expression of ORs that detect food volatiles. We conclude that sulfakinin signaling via SkR1, modulating OR expressions and leading to altered antenna sensitivities, is an important component in starvation-dependent behavioral change.