Neural circuit mechanisms of sexual receptivity in Drosophila females

• Published in: Nature (London) Vol. 589; no. 7843; pp. 577 - 581
• Main Authors: Wang, Kaiyu, Wang, Fei, Forknall, Nora, Yang, Tansy, Patrick, Christopher, Parekh, Ruchi, Dickson, Barry J.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 28.01.2021; Nature Publishing Group
• Subjects: 13/51; 14/19; 14/32; 14/69; 631/378/1804; 631/378/2619; 631/378/3920; 64/24; 9/74; Abdomen; Acoustic Stimulation; Animal reproduction; Animals; Auditory Pathways; Circuits; Copulation; Courtship; Decisions; Drosophila; Drosophila melanogaster - cytology; Drosophila melanogaster - physiology; Female; Females; Fruit flies; Humanities and Social Sciences; Insects; Male; Males; Mating; Mating Preference, Animal; multidisciplinary; Neural circuitry; Neural networks; Neural Pathways - cytology; Neural Pathways - physiology; Neurons; Neurons - physiology; Optogenetics; Peptides; Physiological aspects; Science; Science (multidisciplinary); Sexual behavior; Sexual receptivity; Song; Sperm; Vagina; Vocalization, Animal; United States
• ISSN: 0028-0836; 1476-4687; 1476-4687
• DOI: 10.1038/s41586-020-2972-7

Choosing a mate is one of the most consequential decisions a female will make during her lifetime. A female fly signals her willingness to mate by opening her vaginal plates, allowing a courting male to copulate 1 , 2 . Vaginal plate opening (VPO) occurs in response to the male courtship song and is dependent on the mating status of the female. How these exteroceptive (song) and interoceptive (mating status) inputs are integrated to regulate VPO remains unknown. Here we characterize the neural circuitry that implements mating decisions in the brain of female Drosophila melanogaster . We show that VPO is controlled by a pair of female-specific descending neurons (vpoDNs). The vpoDNs receive excitatory input from auditory neurons (vpoENs), which are tuned to specific features of the D. melanogaster song, and from pC1 neurons, which encode the mating status of the female 3 , 4 . The song responses of vpoDNs, but not vpoENs, are attenuated upon mating, accounting for the reduced receptivity of mated females. This modulation is mediated by pC1 neurons. The vpoDNs thus directly integrate the external and internal signals that control the mating decisions of Drosophila females. In Drosophila melanogaster , female mating decisions are governed by female-specific descending neurons that integrate input from auditory neurons that respond to features of the song of a conspecific male and central neurons that encode the mating status of the female.