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Females control the paternity of their offspring by selectively mating with males they perceive to be of high quality. In species where females mate with multiple males in succession, females may bias offspring paternity by favoring the sperm of one male over another, a process known as cryptic female choice. 1 While evidence of cryptic female choice exists in multiple taxa, the mechanisms underlying this process have remained difficult to unravel. 2 Understanding cryptic female choice requires demonstration of a female-driven post-mating bias in sperm use and paternity and a causal link between this bias and male cues. 3 In this study, we present evidence of cryptic female choice in female Drosophila melanogaster. Through experiments utilizing transgenic males expressing fluorescent sperm, we observed that exposure to attractive males between matings prompts females to expel the ejaculate of their initial mate more rapidly than in the presence of less attractive males. While doing so, females exhibit a bias in sperm storage against their first mate, thereby favoring the paternity of their subsequent mate. Our findings reveal that females adjust the timing of ejaculate expulsion in response to male pheromones in their environment, specifically heptanal and 11- cis -vaccenyl acetate, which are sensed by females through specific odorant receptors. We provide a cryptic female choice mechanism allowing a female to modulate the share of paternity of her first mate depending on the sensing of the quality of potential mates in her environment. These findings showcase that paternity can be influenced by events beyond copulation. [Display omitted] • D. melanogaster females exert cryptic mate choice • Females eject their first mate's ejaculate faster in the presence of attractive males • Females exposed to attractive males bias sperm storage against their first mate • Male pheromones heptanal and cVA are sufficient to shorten ejection latency Doubovetzky et al. present evidence of cryptic female choice in Drosophila melanogaster. Females exposed to pheromones of attractive males expedite ejaculate ejection from their first mate, favoring subsequent mates' sperm. This work highlights that female fruit flies can influence paternity of their offspring through post-copulatory mechanisms. [ABSTRACT FROM AUTHOR]

Being part of a group facilitates cooperation between group members but also creates competition for resources. This is a conundrum for gravid females, whose future offspring benefit from being in a group only if there are enough resources relative to group size. Females may therefore be expected to modulate reproductive output depending on social context. In the fruit fly Drosophila melanogaster , females actively attract conspecifics to lay eggs on the same resources, generating groups in which individuals may cooperate or compete. The genetic tractability of this species allows dissecting the mechanisms underlying physiological adaptation to social context. Here, we show that females produce eggs increasingly faster as group size increases. By laying eggs faster when grouped than when isolated, females reduce competition between offspring and increase offspring survival. In addition, grouped females lay eggs during the day, while isolated females lay them at night. We show that responses to the presence of others requires visual input and that flies from any sex, mating status, or species can trigger these responses. The mechanisms of this modulation of egg laying by group is connected to a lifting of the inhibition of light on oogenesis and egg laying, possibly mediated in part by an increase in juvenile hormone activity. Because modulation of reproduction by social context is a hallmark of animals with higher levels of sociality, our findings in a species considered solitary question the validity of this nomenclature and suggest a widespread and profound influence of social context on reproduction. [Display omitted] • Light inhibits egg laying in isolated, but not in grouped, females • Presence of other flies lifts light's inhibition of oogenesis and ovulation • Females speed egg-laying onset in a group to ensure offspring survival • D. melanogaster 's reproduction is fundamentally influenced by social context Bailly et al. show that being grouped induces fruit fly females to lay eggs through the day and night, while isolated females lay eggs at night. Females detect others via vision, which results in faster oogenesis during the day, likely mediated by juvenile hormone. Reproduction in fruit flies is thus fundamentally modulated by the presence of others. [ABSTRACT FROM AUTHOR]