A novel sex difference in Drosophila contact chemosensory neurons unveiled using single cell labeling

Abstract

Among the sensory modalities involved in controlling mating behavior in Drosophila melanogaster, contact sex pheromones play a primary role. The key receptor neurons for contact sex pheromones are located on the forelegs, which are activated in males upon touching the female abdomen during tapping events in courtship actions. A fruitless (fru)-positive (fru [+]) male-pheromone sensing cell (M-cell) and a fru [+] female-pheromone sensing cell (F-cell) are paired in a sensory bristle on the legs, and some fru [+] chemoreceptor axons project across the midline in the thoracic neuromere in males but not in females. However, the receptor cells that form sexually dimorphic axon terminals in the thoracic ganglia remain unknown. By generating labeled single-cell clones, we show that only a specific subset of fru [+] chemosensory neurons have axons that cross the midline in males. We further demonstrate that there exist two male-specific bristles, each harboring two chemosensory neurons; neither of which exhibits midline crossing, a masculine characteristic. This study reveals hitherto unrecognized sex differences in chemosensory neurons, imposing us to reinvestigate the pheromone input pathways that impinge on the central courtship circuit.

Keywords:

• Sexual dimorphism
• pheromone reception
• sensory bristles
• gustatory neurons
• MARCM

Acknowledgement

We thank B. J. Dickson, M. Noll, the Bloomington Drosophila Stock Center, Kyoto Stock Center (DGRC) at Kyoto Institute of Technology, and the Vienna Drosophila Resource Center for fly stocks and A. Izumi and T. Koizumi for technical assistance.

Disclosure statement

No potential conflict of interest was reported by the authors.

Additional information

Funding

This work was supported, in part, by Grants-in-Aid for Scientific Research [Nos. 17K19371, 17H05935 and 16H06371 to D.Y. and 18K06326 and 16H06371 to K-I.K.) from MEXT.