Abstract

BackgroundSub-optimal developmental diets often have adverse effects on long-term fitness and health. One hypothesis is that such effects are caused by mismatches between the developmental and adult environment, and may be mediated by persistent changes in gene expression. However, there are few experimental tests of this hypothesis. Here we address this using the fruit fly, Drosophila melanogaster. We vary diet during development and adulthood in a fully factorial design and assess the consequences for both adult life history traits and gene expression at middle and old age.ResultsWe find no evidence that mismatches between developmental and adult diet are detrimental to either lifespan or fecundity. Rather, developmental and adult diet exert largely independent effects on both lifespan and gene expression, with adult diet having considerably more influence on both traits. Furthermore, we find effects of developmental diet on the transcriptome that persist into middle and old-age. Most of the genes affected show no correlation with the observed phenotypic effects of larval diet on lifespan. However, in each sex we identify a cluster of ribosome, transcription, and translation-related genes whose expression is altered across the lifespan and negatively correlated with lifespan.ConclusionsAs several recent studies have linked decreased expression of ribosomal and transcription related proteins to increased lifespan, these provide promising candidates for mediating the effects of larval diet on lifespan. We place our findings in the context of theories linking developmental conditions to late-life phenotypes and discuss the likelihood that gene expression differences caused by developmental exposure causally relate to adult ageing phenotypes.

Highlights

  • Sub-optimal developmental diets often have adverse effects on long-term fitness and health

  • The 0.25SY larval diet tended to increase lifespan across adult diets, while the 2.5SY larval diet decreased it (Fig. 2a,b; p-values for all pairwise comparisons between larval diets given in Additional file 1: S1)

  • We found that for the most part larval and adult diet exert independent effects on the phenotype and on gene expression, and there is no evidence for Programming or Predictive Adaptive Responses operating in Drosophila melanogaster

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Summary

Introduction

Sub-optimal developmental diets often have adverse effects on long-term fitness and health. One hypothesis is that such effects are caused by mismatches between the developmental and adult environment, and may be mediated by persistent changes in gene expression. The quality or quantity of available nutrition is a major factor affecting the life history of an organism [1, 2]. The reigning paradigm for studying the effects of nutrition on life histories has been to manipulate diet quality or quantity in a single life stage The phenotypic changes that result from environmental conditions in an earlier life stage can Theories that attempt to link developmental and adult dietary conditions to adult phenotypic variation include the silver spoon [10], the developmental programming [11], and the predictive adaptive response hypotheses [12, 13]. Similar effects have been observed across a broad range of taxa including birds, insects, and mammals [7, 8, 14, 15]

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