Contact Chemoreceptors Mediate Male-Male Repulsion and Male-Female Attraction during Drosophila Courtship

The elaborate courtship ritual of Drosophila males is dictated by neural circuitry established by the transcription factor Fruitless and triggered by sex-specific sensory cues. Deciphering the role of different stimuli in driving courtship behavior has been limited by the inability to selectively target appropriate sensory classes. Here, we identify two ion channel genes belonging to the degenerin/epithelial sodium channel/pickpocket (ppk) family, ppk23 and ppk29, which are expressed in fruitless-positive neurons on the legs and are essential for courtship. Gene loss-of-function, cell-inactivation, and cell-activation experiments demonstrate that these genes and neurons are necessary and sufficient to inhibit courtship toward males and promote courtship toward females. Moreover, these cells respond to cuticular hydrocarbons, with different cells selectively responding to male or female pheromones. These studies identify a large population of pheromone-sensing neurons and demonstrate the essential role of contact chemosensation in the early courtship steps of mate selection and courtship initiation. [Display omitted] ► ppk23 and ppk29 ion channels are expressed in chemosensory neurons ► ppk23 is necessary for inhibition of courtship to males ► ppk23 and ppk29 are necessary for promoting courtship to females ► ppk23 cells respond to male or female pheromones The tendency of male flies to avoid other males and select females for courtship depends on ion channel genes expressed in gustatory neurons within the leg. Distinct subsets of these neurons respond to contact with male- or female-specific cuticular hydrocarbons.