Modest dietary restriction (DR) prolongs life in a wide range of organisms, spanning single-celled yeast to mammals. Here, we report the use of recent techniques in nutrition research to quantify the detailed relationship between diet, nutrient intake, lifespan, and reproduction in Drosophila melanogaster. Caloric restriction (CR) was not responsible for extending lifespan in our experimental flies. Response surfaces for lifespan and fecundity were maximized at different protein-carbohydrate intakes, with longevity highest at a protein-to-carbohydrate ratio of 1:16 and egg-laying rate maximized at 1:2. Lifetime egg production, the measure closest to fitness, was maximized at an intermediate P:C ratio of 1:4. Flies offered a choice of complementary foods regulated intake to maximize lifetime egg production. The results indicate a role for both direct costs of reproduction and other deleterious consequences of ingesting high levels of protein. We unite a body of apparently conflicting work within a common framework and provide a platform for studying aging in all organisms.diet restriction ͉ geometric framework ͉ longevity ͉ nutrition ͉ aging A nimals that eat less live longer-up to a point. The view that dietary restriction without malnutrition prolongs life has become a central tenet in gerontology (1-3). Yeasts, fruit flies, nematode worms, and mice have become model systems for studying dietary restriction and aging, with some striking commonalities evident at the molecular and cellular levels (1-6). There is growing interest in the relationship between dietary restriction and quality and length of life in humans, although experimental data are lacking and difficult to obtain (7).It is widely held that the life-extending effects of dietary restriction (DR) are due to caloric restriction (CR) (1,8,9), but recently this view has been challenged by experiments suggesting that specific nutrients (proteins and certain amino acids) rather than energy are responsible (10-12). Claims and counterclaims in the debate over the roles of energy and specific nutrients in aging (8,(11)(12)(13)(14) have been hampered by one or more of the following problems (15). First, there is a lack of a suitable concept for baseline energy and nutrient intake, that is, dietary restriction relative to what? Thus, it may be that diet-restricted animals live longer either because eating less extends life, or because the normal nutritional regime in the laboratory is harmfully nutrient-rich in relation to requirements (15-17). Second, there have been too few dietary treatments used within an experiment to allow the effects of nutrients and energy to be partitioned. Hence, data from studies on rodents and Drosophila, which are claimed to prove the primacy of calories in influencing longevity, are open to alternative explanations (15). Finally, in the notable case of Drosophila, no study to date has measured how much flies actually eat throughout their lives. Rather, dietary restriction has been assumed to have occurred after dilution of the di...
Summary 1.Mounting an immune response is likely to be costly in terms of energy and nutrients, and so it is predicted that dietary intake should change in response to infection to offset these costs. The present study focuses on the interactions between a specialist grass-feeding caterpillar species, the African armyworm Spodoptera exempta , and an opportunist bacterium, Bacillus subtilis . 2.The main aims of the study were (i) to establish the macronutrient costs to the insect host of surviving a systemic bacterial infection, (ii) to determine the relative importance of dietary protein and carbohydrate to immune system functions, and (iii) to determine whether there is an adaptive change in the host's normal feeding behaviour in response to bacterial challenge, such that the nutritional costs of resisting infection are offset. 3. We show that the survival of bacterially infected larvae increased with increasing dietary protein-to-carbohydrate (P:C) ratio, suggesting a protein cost associated with bacterial resistance. As dietary protein levels increased, there was an increase in antibacterial activity, phenoloxidase (PO) activity and protein levels in the haemolymph, providing a potential source for this protein cost. However, there was also evidence for a physiological trade-off between antibacterial activity and phenoloxidase activity, as larvae whose antibacterial activity levels were elevated in response to immune activation had reduced PO activity. 4. When given a choice between two diets varying in their P:C ratios, larvae injected with a sub-lethal dose of bacteria increased their protein intake relative to control larvae whilst maintaining similar carbohydrate intake levels. These results are consistent with the notion that S. exempta larvae alter their feeding behaviour in response to bacterial infection in a manner that is likely to enhance the levels of protein available for producing the immune system components and other factors required to resist bacterial infections ('self-medication').
Abstract. The interactive effects of macronutrient balance [protein (P) : carbohydrate (C) ratio] and dietary dilution by cellulose on nutritional regulation and performance were investigated in the generalist caterpillar Spodoptera littoralis (Boisduval). Caterpillars were reared through the final stadium on one of 20 foods varying factorially in macronutrient content (P + C%: 42, 33.6. 25.2 or 16.8%) and P : C ratio (5 : 1, 2 : 1, 1 : 1, 1 : 2 or 1 : 5). The animals compensate by eating more of diluted foods, but suffer reduced nutrient intake in proportion to the degree of dilution. Increase in food intake with dilution is greater on balanced than imbalanced foods and this is reflected in greater reduction of dry pupal mass with dilution in the latter. Whereas dilution results in a reduction in the amount of whichever macronutrient is in excess in the food, by contrast, the ability to compensate for the deficient macronutrient in the food is unaffected by nutrient imbalance. Excess protein intake due to nutritional imbalance (diets with high P : C ratios) results in a regulatory decrease in the efficiency of retention of ingested nitrogen relative to restricted protein intake on oppositely imbalanced foods (low P : C ratios). By contrast, decreased protein intake due to dietary dilution is associated with a non‐regulatory reduction in the efficiency of retention, irrespective of P : C ratio. Dilution is similarly associated with reduced utilization efficiency of ingested carbohydrate. The ecological implications of these results are discussed.
Temperature and nutrition are two prominent environmental variables influencing juvenile growth rate in ectotherms. These two factors interact in complex ways. Here, we present a comprehensive analysis of the interactive effects of temperature and nutrition on various components of fitness (growth rate, survival), food intake, and level of energy storage in an insect herbivore, caterpillars of Spodoptera exigua Hübner (Lepidoptera: Noctuidae). In a factorial experimental design, final‐instar caterpillars (i.e., fifth instars) were individually reared at one of three constant temperatures (18, 26, and 34 °C), in which they received one of six diets differing in their ratio of protein and digestible carbohydrate [P:C mixture, expressed as the percentage of diet by dry mass: protein 42%:carbohydrate 0% (42:0), 35:7, 28:14, 21:21, 14:28, and 7:35]. Within the range of test temperatures, larval growth rate increased with rising temperature and was strongly affected by P:C mixture, reaching a maximum on moderate P:C diets at each temperature and falling at very high and low P:C mixtures. There was a significant temperature*diet interaction, such that the difference in growth rates between temperatures was greatest on moderate P:C diets and least on the most extreme diets (42:0 and 7:35). Food intake rate patterns followed a similar trend to growth rate. Rapidly growing animals at high ambient temperature suffered high mortality across all dietary P:C mixtures, but to a greater extent on the extremely unbalanced diets. This suggests that there are developmental and physiological costs associated with fast growth at high temperature, as indicated by high rate of pupation failure and reduced lipid storage efficiency. Our study shows how temperature and nutrition interplay to mediate phenotypic variations in growth rates and energy utilization in an insect ectotherm.
Failure to adapt to a changing nutritional environment comes at a cost, as evidenced by the modern human obesity crisis. Consumption of energy-rich diets can lead to obesity and is associated with deleterious consequences not only in humans but also in many other animals, including insects. The question thus arises whether animals restricted over multiple generations to high-energy diets can evolve mechanisms to limit the deposition of adverse levels of body fat. We show that Plutella xylostella caterpillars reared for multiple generations on carbohydrate-rich foods (either a chemically defined artificial diet or a high-starch Arabidopsis mutant) progressively developed the ability to eat excess carbohydrate without laying it down as fat, providing strong evidence that excess fat storage has a fitness cost. In contrast, caterpillars reared in carbohydrate-scarce environments (a chemically defined artificial diet or a low-starch Arabidopsis mutant) had a greater propensity to store ingested carbohydrate as fat. Additionally, insects reared on the low-starch Arabidopsis mutant evolved a preference for laying their eggs on this plant, whereas those selected on the high-starch Arabidopsis mutant showed no preference. Our results provide an experimental example of metabolic adaptation in the face of changes in the nutritional environment and suggest that changes in plant macronutrient profiles may promote hostassociated population divergence.geometric framework ͉ nutrition ͉ Plutella
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