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A Neural Circuit Controlling Virgin Female Aggression Induced by Mating-related Cues in Drosophila.

ABSTRACT: Females increase aggression for mating opportunities and for acquiring reproductive resources. Although the close relationship between female aggression and mating status is widely appreciated, whether and how female aggression is regulated by mating-related cues remains poorly understood. Here we report an interesting observation that Drosophila virgin females initiate high-frequency attacks toward mated females. We identify 11-cis-vaccenyl acetate (cVA), a male-derived pheromone transferred to females during mating, which promotes virgin female aggression. We subsequently reveal a cVA-responsive neural circuit consisting of four orders of neurons, including Or67d, DA1, aSP-g, and pC1 neurons, that mediate cVA-induced virgin female aggression. We also determine that aSP-g neurons release acetylcholine (ACh) to excite pC1 neurons via the nicotinic ACh receptor nAChRα7. Together, beyond revealing cVA as a mating-related inducer of virgin female aggression, our results identify a neural circuit linking the chemosensory perception of mating-related cues to aggressive behavior in Drosophila females.

SUBMITTER: Wan X

PROVIDER: S-EPMC10465459 | biostudies-literature | 2023 Sep

REPOSITORIES: biostudies-literature

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A Neural Circuit Controlling Virgin Female Aggression Induced by Mating-related Cues in Drosophila.

Wan Xiaolu X Shen Peng P Shi Kai K Li Jing J Wu Fengming F Zhou Chuan C

Neuroscience bulletin 20230321 9

Females increase aggression for mating opportunities and for acquiring reproductive resources. Although the close relationship between female aggression and mating status is widely appreciated, whether and how female aggression is regulated by mating-related cues remains poorly understood. Here we report an interesting observation that Drosophila virgin females initiate high-frequency attacks toward mated females. We identify 11-cis-vaccenyl acetate (cVA), a male-derived pheromone transferred to ...[more]

PMID: 36941515

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Project description:Appropriate displays of aggression rely on the ability to recognize potential competitors. As in most species, Drosophila males fight with other males and do not attack females. In insects, sex recognition is strongly dependent on chemosensory communication, mediated by cuticular hydrocarbons acting as pheromones. While the roles of chemical and other sensory cues in stimulating male to female courtship have been well characterized in Drosophila, the signals that elicit aggression remain unclear. Here we show that when female pheromones or behavior are masculinized, males recognize females as competitors and switch from courtship to aggression. To masculinize female pheromones, a transgene carrying dsRNA for the sex determination factor transformer (traIR) was targeted to the pheromone producing cells, the oenocytes. Shortly after copulation males attacked these females, indicating that pheromonal cues can override other sensory cues. Surprisingly, masculinization of female behavior by targeting traIR to the nervous system in an otherwise normal female also was sufficient to trigger male aggression. Simultaneous masculinization of both pheromones and behavior induced a complete switch in the normal male response to a female. Control males now fought rather than copulated with these females. In a reciprocal experiment, feminization of the oenocytes and nervous system in males by expression of transformer (traF) elicited high levels of courtship and little or no aggression from control males. Finally, when confronted with flies devoid of pheromones, control males attacked male but not female opponents, suggesting that aggression is not a default behavior in the absence of pheromonal cues. Thus, our results show that masculinization of either pheromones or behavior in females is sufficient to trigger male-to-female aggression. Moreover, by manipulating both the pheromonal profile and the fighting patterns displayed by the opponent, male behavioral responses towards males and females can be completely reversed. Therefore, both pheromonal and behavioral cues are used by Drosophila males in recognizing a conspecific as a competitor.

Project description:Competition over access to resources early in life can influence development, and, in turn, affect competitive phenotypes in reproductive adults. Theory predicts that competition between adult females should be especially context-dependent, because of constraints imposed by high costs of reproduction. However, the potential impact of developmental environments on competition in adult females remains little understood.In Drosophila melanogaster, the developmental environment can strongly influence adult condition, and prime adult competitive behaviour. In this species, female-female aggression is dependent on reproductive state and increases after mating due to the receipt of sperm and seminal fluid components. However, the effects of the developmental environment on adult female aggression, and any potential interactions with mating status, are unknown.To address this problem, we first raised flies at low and high larval density, which altered competition over limited resources, produced large and small adult females, respectively, and potentially primed them for differing levels of adult competition. We then fought the resulting adult females, either as virgins, or after receiving aggression-stimulating ejaculates at mating, to test for interacting effects.We found, as expected, that mating elevated contest duration. However, this mating-induced boost in aggression was strongly exacerbated for high density (small) females. Low density (large) females won more contests overall, but were not more successful in fights after mating. In contrast, mating increased the fighting success in females raised in high density environments.Our results suggest that individuals who experience competitive, resource-limited, rearing conditions are more sensitive to the aggression-stimulating effects of the male ejaculate. This finding highlights the importance of the developmental environment in mediating adult social interactions and provides support for the theory that female-female aggression should be highly context-dependent. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13214/suppinfo is available for this article.

Dataset Information

A Neural Circuit Controlling Virgin Female Aggression Induced by Mating-related Cues in Drosophila.

Publications

A Neural Circuit Controlling Virgin Female Aggression Induced by Mating-related Cues in Drosophila.

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