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A resource-poor developmental diet reduces adult aggression in male Drosophila melanogaster

ABSTRACT: Aggressive behaviours occur throughout the animal kingdom and agonistic contests often govern access to resources. Nutrition experienced during development has the potential to influence aggressive behaviours in adults through effects on growth, energy budgets and an individual’s internal state. In particular, resource-poor developmental nutrition might decrease adult aggression by limiting growth and energy budgets, or alternatively might increase adult aggression by enhancing motivation to compete for resources. However, the direction of this relationship—and effects of developmental nutrition experienced by rivals—remains unknown in most species, limiting understanding of how early-life environments contribute to variation in aggression. We investigated these alternative hypotheses by assessing male-male aggression in adult fruit flies, Drosophila melanogaster, that developed on a low-, medium- or high-resource diet, manipulated via yeast content. We found that a low-resource developmental diet reduced the probability of aggressive lunges in adults, as well as threat displays against rivals that developed on a low-resource diet. These effects appeared to be independent of diet-related differences in body mass. Males performed relatively more aggression on a central food patch when facing rivals of a low-resource diet, suggesting that developmental diet affects aggressive interactions through social effects in addition to individual effects. Our finding that resource-poor developmental diets reduce male-male aggression in D. melanogaster is consistent with the idea that resource budgets mediate aggression and in a mass-independent manner. Our study improves understanding of the links between nutrition and aggression. Significance statement Early-life nutrition can influence social behaviours in adults. Aggression is a widespread social behaviour with important consequences for fitness. Using the fruit fly, Drosophila melanogaster, we show that a poor developmental diet reduces aspects of adult aggressive behaviour in males. Furthermore, males perform more aggression near food patches when facing rivals of poor nutrition. This suggests that early-life nutrition affects aggressive interactions through social effects in addition to individual effects.

Supplementary Information

The online version contains supplementary material available at 10.1007/s00265-021-03050-z.

SUBMITTER: Edmunds D

PROVIDER: S-EPMC8549984 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Males of many species fine-tune their ejaculates in response to sperm competition risk. Resource availability and the number of competitors during development can also strongly influence sperm production. However, despite the key role of seminal proteins in mediating reproductive processes, it is unclear whether seminal protein investment is dependent on the developmental environment.We manipulated the developmental environment of Drosophila melanogaster by rearing flies at low and high density. As expected, this resulted in large and small (i.e. high and low condition) adult phenotypes, respectively.As predicted, large males produced more of two key seminal proteins, sex peptide (SP) and ovulin, and were more successful at obtaining matings with both virgin and previously mated females. However, there was only a weak and non-significant trend for large males to transfer more absolute quantities of SP at mating, and thus, small males ejaculated proportionally more of their stored accessory gland SP resources.Males transferred more receptivity-inhibiting SP to large females. Despite this, large females remated more quickly than small females and thus responded to their developmental environment over and above the quantity of SP they received.The results are consistent with two non-mutually exclusive hypotheses. First, flies might respond to condition-dependent reproductive opportunities, with (i) small males investing heavily in ejaculates when mating opportunities arise and large males strategically partitioning SP resources and (ii) small females remating at reduced rates because they have higher mating costs or need to replenish sperm less often.Second, flies may be primed by their larval environment to deal with similar adult population densities, with (i) males perceiving high density as signalling increased competition, leading small males to invest proportionally more SP resources at mating and (ii) females perceiving high density as signalling abundant potential mates, leading to a higher sexual receptivity threshold.Thus, by influencing the mating frequencies of both sexes, as well as the quantity of seminal proteins produced by males and received by females, the developmental environment is likely to have far-reaching and sex-specific consequences for sexual selection and sexual conflict.

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.

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A resource-poor developmental diet reduces adult aggression in male Drosophila melanogaster

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