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Cell types and neuronal circuitry underlying female aggression in Drosophila.

ABSTRACT: Aggressive social interactions are used to compete for limited resources and are regulated by complex sensory cues and the organism's internal state. While both sexes exhibit aggression, its neuronal underpinnings are understudied in females. Here, we identify a population of sexually dimorphic aIPg neurons in the adult Drosophila melanogaster central brain whose optogenetic activation increased, and genetic inactivation reduced, female aggression. Analysis of GAL4 lines identified in an unbiased screen for increased female chasing behavior revealed the involvement of another sexually dimorphic neuron, pC1d, and implicated aIPg and pC1d neurons as core nodes regulating female aggression. Connectomic analysis demonstrated that aIPg neurons and pC1d are interconnected and suggest that aIPg neurons may exert part of their effect by gating the flow of visual information to descending neurons. Our work reveals important regulatory components of the neuronal circuitry that underlies female aggressive social interactions and provides tools for their manipulation.

SUBMITTER: Schretter CE

PROVIDER: S-EPMC7787668 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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Cell types and neuronal circuitry underlying female aggression in <i>Drosophila</i>.

Schretter Catherine E CE Aso Yoshinori Y Robie Alice A AA Dreher Marisa M Dolan Michael-John MJ Chen Nan N Ito Masayoshi M Yang Tansy T Parekh Ruchi R Branson Kristin M KM Rubin Gerald M GM

eLife 20201103

Aggressive social interactions are used to compete for limited resources and are regulated by complex sensory cues and the organism's internal state. While both sexes exhibit aggression, its neuronal underpinnings are understudied in females. Here, we identify a population of sexually dimorphic aIPg neurons in the adult <i>Drosophila melanogaster</i> central brain whose optogenetic activation increased, and genetic inactivation reduced, female aggression. Analysis of GAL4 lines identified in an ...[more]

PMID: 33141021

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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

Cell types and neuronal circuitry underlying female aggression in Drosophila.

Publications

Cell types and neuronal circuitry underlying female aggression in <i>Drosophila</i>.

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