Are there dedicated female neurons for saying no to sex? In the sophisticated fly Drosophila, there are.

Neuroscience: The Female Art of Saying No. Anne C.von Philipsborn. Current Biology, Volume 30, Issue 19, October 5 2020, Pages R1080-R1083. https://doi.org/10.1016/j.cub.2020.08.023

Rolf Degen's take: https://twitter.com/DegenRolf/status/1313135084627783682

Refers to: Ovipositor Extrusion Promotes the Transition from Courtship to Copulation and Signals Female Acceptance in Drosophila melanogaster. Cecilia Mezzera, Margarida Brotas, Miguel Gaspar, Hania J. Pavlou, Stephen F. Goodwin, Maria Luísa Vasconcelos. Current Biology, Volume 30, Issue 19, October 5 2020, Pages 3736-3748.e5. https://www.sciencedirect.com/science/article/abs/pii/S0960982220311775

Summary: Females communicate sexual receptivity in various ways. Drosophila signal that they are mated and ovulating, and resistive to mating again, by extruding their egg-laying organ (ovipositor). Connectome-aided circuit analysis reveals how this break up message is computed and differs from an acceptance response in virgins.

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Are there dedicated female neurons for saying no to sex? In the sophisticated fly Drosophila, there are.

From the Mezzera paper:

Summary: 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.

Discussion

The transition from courtship to copulation is a critical moment for the reproductive success of animals. The exact steps leading to this transition in any species remain largely uncharacterized [41]. In our work, we showed that in fruit flies, male licking and female ovipositor extrusion are involved in this transition (schema in Figure 5G). An important feature of this interaction is that the female mating status determines whether this transition is complete. We observed that virgin females retract the ovipositor upon a male’s attempt, thus allowing copulation, whereas mated females do not, thus blocking copulation.

Virgin and mated females use a variation of the same behavior to stimulate and prevent copulation, respectively. This variation requires different descending neurons probably acting on common circuits. This could be a versatile and economic strategy to mediate opposite responses when the same individual uses one or the other variation depending on the circumstances.

Why would a mated female signal the male to attempt copulation while blocking intromission? In circumstances that we have not addressed in this study, mated females re-mate. For a few hours after mating, and given the appropriate context, mated females will eject the sperm and re-mate in an attempt to increase fecundity and offspring genetic diversity [25, 42]. In this case, prompting the male to attempt copulation makes sense, as it could lead to copulation. An additional role for full ovipositor extrusion in mated females, which we have not explored here, may be in announcing the female’s current pheromonal composition. Ovipositor extrusion would be an efficient way of exposing the anti-aphrodisiac pheromones 3-O-acetyl-1,3-dihydroxyoctacosa-11,19-diene [24] present in the tip of the ovipositor and cis-vaccenyl acetate, mostly in the reproductive system [25, 43], which, together with 7-tricosene [23] present in the cuticle, indicate to an approaching male that the female has mated, and, depending on the combination and intensity of the chemical cues, the male may or may not initiate courtship.

In this work, we identified a pair of descending neurons that control full ovipositor extrusion. Full ovipositor extrusion can be induced in the virgin female by DNp13 activation, but activity in these neurons is not necessary for ovipositor extrusion in virgins. Although full and partial ovipositor extrusions do not have a sharp distinction, ovipositor extrusion is commanded by different neurons and controlled differently in virgin and mated flies. It remains to be elucidated which are the descending neurons controlling virgin ovipositor extrusion and how they interact with DNp13 to control similar behavior in females in different mating states.

Our work shows that, during the interaction between the sexes, the female responds to the male courtship song with ovipositor extrusion. However, it is apparent in the videos that song does not always lead to ovipositor extrusion. This response pattern suggests that ovipositor extrusion is not a reflexive reaction to courtship song, but rather arises from a temporal or multimodal integration. Further experiments are required to elucidate the nature of this association. How does the male verify that the song was heard? Our results indicate that the male is sampling the female genitalia with the proboscis throughout courtship. Presumably, licking is intended to probe the chemical landscape of the female genitalia, which is likely to change when the ovipositor is extruded; in this way, the male could sense when the female is responding to the song. We show that licking of the ovipositor elicits a copulation attempt. In line with early suggestions that compounds are released during ovipositor extrusion to stimulate the male [11], we speculate that a chemical compound is presented with the ovipositor by the female and sensed by taste neurons on the male proboscis. A gustatory signal, yet unidentified and common to virgin and mated females, would stimulate the male to attempt copulation. Having established that licking an extruded ovipositor is the starting point for the male to attempt copulation allows us to use the same starting point to study how the transition from courtship to copulation is processed in the male brain.

In conclusion, our work highlights how both sexes contribute to continuous communication during courtship that culminates in copulation attempt gated by the female ovipositor extrusion. Moreover, our findings open new avenues of study of the neuronal regulation of behaviors that lead to the transition from courtship to copulation and how this transition regulates neuronal activity.