Ovipositor Extrusion Promotes the Transition from Courtship to Copulation and Signals Female Acceptance in Drosophila melanogaster

• Published in: Current biology Vol. 30; no. 19; pp. 3736 - 3748.e5
• Main Authors: Mezzera, Cecilia, Brotas, Margarida, Gaspar, Miguel, Pavlou, Hania J., Goodwin, Stephen F., Vasconcelos, Maria Luísa
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 05.10.2020
• Subjects: Animals; Copulation - physiology; Courtship; courtship behavior; descending neurons; doublesex; Drosophila melanogaster; Drosophila melanogaster - anatomy & histology; Female; female decision; Genitalia, Female - physiology; Male; motor output; Oviposition - physiology; ovipositor extrusion; sexual behavior; Sexual Behavior, Animal - physiology; female decision; descending neurons; motor output; sexual behavior; ovipositor extrusion; doublesex; courtship behavior; Drosophila melanogaster
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2020.06.071

Communication between male and female fruit flies during courtship is essential for successful mating, but, as with many other species, it is the female who decides whether to mate. Here, we show a novel role for ovipositor extrusion in promoting male copulation attempts in virgin and mated females and signaling acceptance in virgins. We first show that ovipositor extrusion is only displayed by sexually mature females, exclusively during courtship and in response to the male song. We identified a pair of descending neurons that controls ovipositor extrusion in mated females. Genetic silencing of the descending neurons shows that ovipositor extrusion stimulates the male to attempt copulation. A detailed behavioral analysis revealed that during courtship, the male repeatedly licks the female genitalia, independently of ovipositor extrusion, and that licking an extruded ovipositor prompts a copulation attempt. However, if the ovipositor is not subsequently retracted, copulation is prevented, as it happens with mated females. In this study, we reveal a dual function of the ovipositor: while its extrusion is necessary for initiating copulation by the male, its retraction signals female acceptance. We thus uncover the significance of the communication between male and female that initiates the transition from courtship to copulation. •DNp13 activity induces full ovipositor extrusion•Ovipositor extrusion is a response to the male courtship song•Male licking an extruded ovipositor prompts copulation attempt•Upon copulation attempt, receptive females retract the ovipositor to allow copulation Mezzera et al. uncover the significance of the communication between male and female that initiates the transition from courtship to copulation. A dual function of the fruit fly ovipositor is revealed: while its extrusion is necessary for initiating copulation by the male, its retraction signals female acceptance.