Female copulation song is modulated by seminal fluid

Abstract

In most animal species, males and females communicate during sexual behavior to negotiate reproductive investments. Pre-copulatory courtship may settle if copulation takes place, but often information exchange and decision-making continue beyond that point. Here, we show that female Drosophila sing by wing vibration in copula. This copulation song is distinct from male courtship song and requires neurons expressing the female sex determination factor DoublesexF. Copulation song depends on transfer of seminal fluid components of the male accessory gland. Hearing female copulation song increases the reproductive success of a male when he is challenged by competition, suggesting that auditory cues from the female modulate male ejaculate allocation. Our findings reveal an unexpected fine-tuning of reproductive decisions during a multimodal copulatory dialog. The discovery of a female-specific acoustic behavior sheds new light on Drosophila mating, sexual dimorphisms of neuronal circuits and the impact of seminal fluid molecules on nervous system and behavior.

Copulation Song inDrosophila: Do Females Sing to Change Male Ejaculate Allocation and Incite Postcopulatory Mate Choice?

“…[39,40] Males that lack sperm elicit unusual high levels of female singing (Figure 2b,c). [28] The reason for that is unclear. It should be tested if spermless males transfer more seminal fluid or seminal fluid molecules in a more accessible form (unbound to sperm).…”

“…[53] These prominent examples of seminal fluid molecules acting on the female nervous system make it tempting to speculate about a "song releasing seminal fluid factor," which acts as a pheromone, i.e., a secreted chemical factor that affects the behavior of conspecifics. Since impairment of the secondary cells of the male accessory gland abolishes female song, [28] secondary cell products are good candidates. Of note, recent work established that besides producing and processing specific seminal fluid components, [39,40] secondary cells also alter the metabolism and secretion of the main gland cell type and have a critical role in determining the overall composition of seminal fluid.…”

“…[48,49,55,56] Gustatory receptors are expressed there and on the genitalia. [57,58] Since copulation song starts immediately after intromission, [28] sensing of a song releasing factor through local neurons in the reproductive tract might be more likely than an effect via molecules that have entered the circulatory system and thus gained access to the central nervous system. An alternative explanation is that mechanosensation of intromission and seminal fluid transfer elicits female copulation song.…”

“…While male precopulatory courtship has little or no influence on how much females sing in copula, the composition of ejaculate strongly modulates female copulation song. [28] To shed more light on the function of female copulation song, Figure 1. Female copulation song delays remating and could be a signal in mate choice.…”

“…Since a delay in remating can increase the paternity share of the first male, female copulation song was proposed to have an effect on postcopulatory mate choice. [28] Here, we elaborate on tentative mechanisms and functions of female copulation song in Drosophila. In particular, we want to scrutinize the hypothesis that female copulation song acts as signal in postcopulatory mate choice ( Figure 1c).…”