Abstract

Restriction of nutrients in the adult diet extends lifespan across a diverse range of species, but less is known about the long-term effects of developmental dietary restriction. In particular, it is not known whether adult lifespan is influenced by developmental caloric restriction or macronutrient balance. We used the nutritional geometry approach to independently manipulate protein and carbohydrate contents of the larval diet in the neriid fly, Telostylinus angusticollis, and measured adult lifespan. We found that adult male and female lifespan was shortest when larvae were fed a protein restricted diet. Thus, protein restriction in the larval diet has the opposite effect of protein restriction in the adult diet (which prolongs life in this species and across a wide range of taxa). Adult lifespan was unaffected by larval dietary carbohydrate. These patterns persisted after controlling for larval diet effects on adult body size. We propose that larval and adult protein sources are used for distinct metabolic tasks: during development, dietary protein is used to build a durable soma that enhances adult lifespan, although excessive protein consumption partially reverses this effect.

Highlights

  • Restriction of nutrients in the adult diet extends lifespan across a diverse range of species, but less is known about the long-term effects of developmental dietary restriction

  • Adult body size was positively influenced by both protein and carbohydrate concentrations in the larval diet, positively related to the number of adults that emerged per replicate, and negatively related to development time (Table 1b)

  • Larval dietary protein had a positive effect on adult lifespan up to intermediate levels, with flies reared on 11 g/L protein concentration diets living 73% longer on average than flies reared on protein concentrations below 3 g/L

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Summary

Introduction

Restriction of nutrients in the adult diet extends lifespan across a diverse range of species, but less is known about the long-term effects of developmental dietary restriction. During periods of famine the likelihood of successful reproduction is small, and an individual may re-allocate energy to somatic maintenance, ostensibly to increase the chance of surviving until conditions improve[4] This interpretation is challenged by studies showing that lifespan extension is associated with the specific macronutrient composition and balance of the adult diet, rather than overall caloric restriction[5,6,7,8]. We used a nutritional geometry approach[21] to examine the separate and interactive effects of protein and carbohydrate in the larval diet on adult lifespan of the neriid fly Telostylinus angusticollis (Fig. 1) Previous studies in this species have shown that restriction of adult dietary protein increases lifespan by 67%19. Adults were provided with both protein and sugar to test for effects of developmental dietary restriction independently of adult dietary restriction, and focal individuals were housed with a standardised individual of the opposite sex to allow for reproduction

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