Additive and context-dependent effects of developmental and adult diet on life-history traits and their associations in outbred Drosophila melanogaster population
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Life-history traits such as body size, reproduction, survival, and stress resistance are fundamental to an organism’s fitness and are highly influenced by nutritional environments at different life stages. In this study, we used a full factorial experimental design with isocaloric diets varying in protein-to-carbohydrate ratios during both developmental and adult stages to investigate their effects on key life-history traits in an outbred Drosophila melanogaster population. Our results demonstrated significant diet-induced plasticity, with body size predominantly determined by the developmental diet, where flies raised on carbohydrate-rich diets were larger as adults. Fertility, however, was enhanced by protein-rich diets at both developmental and adult stages, emphasizing the role of protein in reproductive success. Lifespan was strongly stage-dependent, with carbohydrate-rich developmental diets extending adult lifespan, while the same diet in adulthood shortened it. Furthermore, starvation resistance was improved by a protein-rich developmental diet, whereas desiccation resistance was enhanced by a carbohydrate-rich adult diet, illustrating distinct stage-specific nutritional effects on stress tolerance. Notably, no interactions were found between developmental and adult diets for any of these traits, suggesting independent and additive effects of nutrition across life stages. Additionally, the relationships between traits, such as body size and fertility or lifespan and reproduction, shifted depending on dietary context, challenging canonical trade-offs and highlighting the plasticity of trait correlations. These findings suggest that the nutritional environment can decouple established life-history trait correlations, contributing to context-dependent evolutionary trajectories. This highlights the need to account for both developmental and adult dietary environments when examining how organisms adapt to changing ecological conditions.
Impact Summary
Our study uncovers how isocaloric diets with varying macronutrient compositions at both developmental and adult stages decouple traditional life-history trait correlations in Drosophila melanogaster, adding new layers of complexity to life-history evolution. Using a large, outbred population and a full factorial design, we show that developmental and adult nutrition independently and additively shape key adult traits, including body size, reproductive output, lifespan, and stress resistance. For instance, a carbohydrate-rich developmental diet increased body size, while protein-rich diets at both stages boosted reproductive output. Notably, carbohydrate-rich adult diets, while reducing lifespan, improved resistance to stressors such as starvation and desiccation.
Since the underlying nutrient-sensing and metabolic pathways are conserved across species, our findings are broadly relevant beyond Drosophila. The ability of nutrition to independently influence traits at different life stages suggests that selection can act flexibly across the life cycle, allowing organisms to adapt more readily to changing ecological conditions.
Crucially, our results uncouple canonical correlations among life-history traits, such as the relationships between body size and fertility, fertility and longevity, and longevity and stress resistance. These associations are not fixed but shift based on dietary context. This highlights the importance of considering both developmental and adult dietary environments in studies of evolutionary adaptation, as these interactions may profoundly influence how organisms respond to ecological change.
