A Neural Circuit Encoding the Experience of Copulation in Female Drosophila

• Published in: Neuron (Cambridge, Mass.) Vol. 102; no. 5; pp. 1025 - 1036.e6
• Main Authors: Shao, Lisha, Chung, Phuong, Wong, Allan, Siwanowicz, Igor, Kent, Clement F., Long, Xi, Heberlein, Ulrike
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 05-06-2019; Elsevier Limited
• Subjects: Abdomen; Animal reproduction; Animals; Brain - metabolism; Brain - physiology; Copulation; Copulation - physiology; copulation effect; Drosophila; Drosophila melanogaster; Drosophila Proteins - metabolism; Drosophila Proteins - physiology; Experiments; Female; female receptivity; Ganglia, Sensory - metabolism; Ganglia, Sensory - physiology; Genotype & phenotype; Hypotheses; Insects; Ion Channels - metabolism; Ion Channels - physiology; Males; Mating; Mating behavior; mating experience; mechanosensation; Mechanotransduction, Cellular - physiology; myoinhibitory peptide; Neural Pathways; Neurons; Neurons - metabolism; Neurons - physiology; piezo; Proteins; reproductive behavior; sex peptide receptor; Sexual Behavior, Animal - physiology; sexual selection; Software; Sperm; Ventral nerve cord; United States > US; California; female receptivity; reproductive behavior; myoinhibitory peptide; mating experience; sexual selection; copulation effect; piezo; mechanosensation; Drosophila melanogaster; sex peptide receptor
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2019.04.009

Female behavior changes profoundly after mating. In Drosophila, the mechanisms underlying the long-term changes led by seminal products have been extensively studied. However, the effect of the sensory component of copulation on the female’s internal state and behavior remains elusive. We pursued this question by dissociating the effect of coital sensory inputs from those of male ejaculate. We found that the sensory inputs of copulation cause a reduction of post-coital receptivity in females, referred to as the “copulation effect.” We identified three layers of a neural circuit underlying this phenomenon. Abdominal neurons expressing the mechanosensory channel Piezo convey the signal of copulation to female-specific ascending neurons, LSANs, in the ventral nerve cord. LSANs relay this information to neurons expressing myoinhibitory peptides in the brain. We hereby provide a neural mechanism by which the experience of copulation facilitates females encoding their mating status, thus adjusting behavior to optimize reproduction.
•Mating non-ejaculatory males induce a copulation effect reducing female receptivity•Activity of LSAN neurons is necessary and sufficient for copulation effect•Neurons expressing mechanosensory channel Piezo relay copulation effect to LSANs•Neurons expressing MIP mediate copulation effect downstream of LSANs
Female fruit flies are less receptive after mating because of ejaculate from previous mating partners and the act of copulation itself. Shao et al. characterize a neural circuit mediating the sensory signals of copulation that lead to reduced female receptivity.