The shaping of male courtship posture by lateralized gustatory inputs to male-specific interneurons

Unilateral wing vibration to generate "love songs" is a hallmark of male courtship posture in Drosophila melanogaster. In contrast, males of some other Drosophila species extend both wings simultaneously during courtship. Thus, the patterns of wing movement vary among species and are under stringent genetic control, although there are few variations among individuals within a single species. These observations prompted the postulation that the proper wing display by courting males of D. melanogaster does not require sensory inputs.

Here we show that when males of D. melanogaster are deprived of gustatory inputs mediated by the sensory neurons expressing the taste receptor gene Gr32a, a close relative to the pheromone receptor gene Gr68a, they often fail to perform unilateral wing extension during courtship because they become unable to keep a wing in the resting position while extending another wing. The tarsal amputation of a foreleg, but not other legs, increased the occurrence of simultaneous wing extension, indicating that Gr32a-expressing cells in this structure are involved in the regulation of courting posture. A similar simultaneous wing extension was also observed in males in which the putative pheromone-binding protein gene Obp57d was inactivated. The axons of Gr32a-expressing cells project to the subesophageal ganglion, where their terminals unilaterally contact mAL, which are male-specific fruitless (fru)-expressing interneurons that have bilateral branches.

Our observations strongly suggest that gustatory pheromone inputs ensure the correct laterality of wing vibration that conforms to the species-specific behavioral pattern.