Abstract

Dietary restriction (DR), limiting calories or specific nutrients without malnutrition, extends lifespan across diverse taxa. Traditionally, this lifespan extension has been explained as a result of diet‐mediated changes in the trade‐off between lifespan and reproduction, with survival favored when resources are scarce. However, a recently proposed alternative suggests that the selective benefit of the response to DR is the maintenance of reproduction. This hypothesis predicts that lifespan extension is a side effect of benign laboratory conditions, and DR individuals would be frailer and unable to deal with additional stressors, and thus lifespan extension should disappear under more stressful conditions. We tested this by rearing outbred female fruit flies (Drosophila melanogaster) on 10 different protein:carbohydrate diets. Flies were either infected with a bacterial pathogen (Pseudomonas entomophila), injured with a sterile pinprick, or unstressed. We monitored lifespan, fecundity, and measures of aging. DR extended lifespan and reduced reproduction irrespective of injury and infection. Infected flies on lower protein diets had particularly poor survival. Exposure to infection and injury did not substantially alter the relationship between diet and aging patterns. These results do not provide support for lifespan extension under DR being a side effect of benign laboratory conditions.

Highlights

  • Nutrition has long been of interest in the field of aging research, due to its potential applications to an ageing human population

  • Stress treatment had a significant effect on survival, with individuals exposed to infection having a greater risk of death compared to control individuals for the duration of the experiment

  • Our results provide a rare test of the predictions of two alternative evolutionary explanations for the commonly observed extension of lifespan in response to dietary restriction (DR)

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Summary

Introduction

Nutrition has long been of interest in the field of aging research, due to its potential applications to an ageing human population (reviewed in Bertozzi et al, 2016; Redman & Ravussin, 2011; Speakman & Mitchell, 2011). A large body of research has focused on using the DR paradigm to try to understand the mechanisms underlying variation in ageing and lifespan The evolutionary basis of the response has been much less well investigated (Raubenheimer et al, 2016; Regan et al, 2020; Travers et al, 2020; Zajitschek et al, 2016). This is surprising given that knowledge of the evolutionary basis of the DR response is important to understanding under what conditions it may be applicable in human health. We test the two main evolutionary explanations for lifespan extension under DR, which make contrasting predictions about how this response should vary across environments

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