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Interactive effects of sex, social environment, dietary restriction, and methionine on survival and reproduction in fruit flies.

ABSTRACT: For the evolution of life histories, the trade-off between survival and reproduction is fundamental. Because sexes optimize fitness in different ways, this trade-off is expected to be resolved differently by males and females. Consequently, the sexes are predicted to respond differently to changes in resource availability. In fruit flies, research on dietary restriction has focused largely on females maintained in the absence of males, thereby neglecting sexual interactions that affect reproductive behavior of both sexes under more natural conditions. Here, we tested for the interactive effects of diet (40, 60, 100, and 300 % of standard yeast concentrations) and social environment (separate-sex vs. mixed-sex groups) on male and female Drosophila melanogaster life histories. Additionally, we evaluated the essential amino acid methionine as an agent that can uncouple the survival-reproduction trade-off. We show sex differences in the effect of social environment on survival patterns, but not on reproductive fitness. In females, yeast had a positive effect on reproduction and a negative effect on survival. In males, yeast had a negative effect on reproduction and the effect on survival depended on the social environment. Methionine reduced survival, but had no effect on reproduction. Our findings highlight the need to include both sexes and to vary social environments in research programs aimed at lifespan extension and call for further evaluation of the fecundity-restoring effect of methionine.

SUBMITTER: Zajitschek F

PROVIDER: S-EPMC3705097 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The past 2 decades have seen fruit flies being widely adopted for research on social behavior and aggression. This fruitful research, however, has not been well tied to fruit flies' natural history. To address this knowledge gap, I conducted a field study. My goal was to inform future research conducted in artificial surroundings, and to inspire new investigations that can rely more heavily on fruit flies' actual natural behavior. My two main novel findings were first, that flies in the field showed significant sociability, as they formed social groups rather than dispersed randomly among fruits of similar quality. Second, males showed fair levels of aggression towards each other as indicated by a lunging rate of 17 per hour, and lower rates of wing threat and boxing. Courtship was the most prominent activity on fruits, with females rejecting almost all males' advances. This resulted in an estimated mating rate of 0.6 per female per day. Flies showed a striking peak of activity early in the mornings, even at cold temperatures, followed by inactivity for much of the day and night. Flies, however, handled well high temperatures approaching 40 °C by hiding away from fruit and concentrating activity in the cooler, early mornings. My field work highlights a few promising lines of future research informed by fruit flies' natural history. Most importantly, we do not understand the intriguing dynamics that generate significant sociability despite frequent aggressive interactions on fruits. Males' responses to female rejection signals varied widely, perhaps because the signals differed in information content perceived by flies but not humans. Finally, flies tolerated cold early mornings perhaps owing to fitness benefits associated with increased mating and feeding opportunities at this time. Flies were adept at handling very high temperatures under the natural daily temperature fluctuations and availability of shelters, and this can inform more realistic research on the effects of global warming on animals in their natural settings.

Project description:Individual responses to dietary variation represent a fundamental component of fitness, and nutritional adaptation can occur over just a few generations. Maternal effects can show marked proximate responses to nutrition, but whether they contribute to longer term dietary adaptation is unclear. Here, we tested the hypotheses that maternal effects: (i) contribute to dietary adaptation, (ii) diminish when dietary conditions are constant between generations, (iii) are trait-specific and (iv) interact with high- and low-quality food. We used experimental evolution regimes in the medfly (Ceratitis capitata) to test these predictions by subjecting an outbred laboratory-adapted population to replicated experimental evolution on either constant high calorie sugar ('A') or low-calorie starch ('S') larval diets, with a standard adult diet across both regimes. We measured the contribution of maternal effects by comparing developmental and adult phenotypes of individuals reared on their own diet with those swapped onto the opposite diet for either one or two generations (high and low maternal effect conditions, respectively), both at the start and after 30 generations of selection. Initially, there were strong maternal effects on female body mass and male mating success but not larval survival. Interestingly, the initial maternal effects observed in female body mass and male mating success showed sex-specific interactions when individuals from high calorie regimes were tested on low calorie diets. However, as populations responded to selection, the effects of maternal provisioning on all traits diminished. The results broadly supported the predictions. They show how the contribution of maternal effects to dietary responses evolves in a context-dependent manner, with significant variation across different fitness-related traits. We conclude that maternal effects can evolve during nutritional adaptation and hence may be an important life history trait to measure, rather than to routinely minimize.

Project description:Dietary restriction (DR), a reduction in the amount of food or particular nutrients eaten, is the most consistent environmental manipulation to extend lifespan and protect against age related diseases. Current evolutionary theory explains this effect as a shift in the resolution of the trade-off between lifespan and reproduction. However, recent studies have questioned the role of reproduction in mediating the effect of DR on longevity and no study has quantitatively investigated the effect of DR on reproduction across species.Here we report a comprehensive comparative meta-analysis of the effect of DR on reproduction. In general, DR reduced reproduction across taxa, but several factors moderated this effect. The effect of DR on reproduction was greater in well-studied model species (yeast, nematode worms, fruit flies and rodents) than non-model species. This mirrors recent results for longevity and, for reproduction, seems to result from a faster rate of decline with decreasing resources in model species. Our results also suggested that not all reproductive traits are affected equally by DR. High and moderate cost reproductive traits suffered a significant reduction with DR, but low cost traits, such as ejaculate production, did not. Although the effect of DR on reproduction was stronger in females than males, this sex difference reduced to near zero when accounting for other co-factors such as the costliness of the reproductive trait. Thus, sex differences in the effect of DR on longevity may be due to a failure to expose males to as complete a range of the costs of reproduction as females.We suggest that to better understand the generality of the effect of DR, future studies should attempt to address the cause of the apparent model species bias and ensure that individuals are exposed to as many of the costs of reproduction as possible. Furthermore, our meta-analytic approach reveals a general shortage of DR studies that record reproduction, particularly in males, as well as a lack of direct side-by-side comparisons of the effect of DR on males and females.

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Interactive effects of sex, social environment, dietary restriction, and methionine on survival and reproduction in fruit flies.

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