Ovipositor extrusion promotes the transition from courtship to copulation and signals female acceptance in Drosophila melanogaster

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 signalling 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 behavioural analysis revealed that while during courtship the male repeatedly licks the female genitalia independently of ovipositor extrusion, 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.