Abstract

Organisms have evolved molecular mechanisms to ensure consistent and invariant phenotypes in the face of environmental fluctuations. Developmental homeostasis is determined by two factors: robustness, which buffers against environmental variations; and developmental stability, which buffers against intrinsic random variations. However, our understanding of these noise-buffering mechanisms remains incomplete. Here, we showed that appropriate glycemic control confers developmental homeostasis in the fruit fly Drosophila. We found that circulating glucose levels are buffered by trehalose metabolism, which acts as a glucose sink in circulation. Furthermore, mutations in trehalose synthesis enzyme (Tps1) increased the among-individual and within-individual variations in wing size. Whereas wild-type flies were largely resistant to changes in dietary carbohydrate and protein levels, Tps1 mutants experienced significant disruptions in developmental homeostasis in response to dietary stress. These results demonstrate that glucose homeostasis against dietary stress is crucial for developmental homeostasis.

Highlights

  • Organisms have evolved molecular mechanisms to ensure consistent and invariant phenotypes in the face of environmental fluctuations

  • Glycogen, and triglyceride (TAG) levels did not change at the level of whole larvae

  • Understanding the impacts of genotype-by-environment interactions is fundamentally important for unraveling the mechanisms that drive developmental homeostasis

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Summary

Introduction

Organisms have evolved molecular mechanisms to ensure consistent and invariant phenotypes in the face of environmental fluctuations. The concept of developmental homeostasis refers to the ability of an organism to maintain phenotypic consistency and reproducible outcomes in response to genetic and environmental variations[1]. Developmental robustness, or microenvironmental canalization, buffers phenotypic variations against genetic and/or environmental conditions[2]. Developmental robustness is commonly evaluated as the phenotypic variations among individuals that share genetic and environmental conditions. The genetic basis of developmental homeostasis has been intensively studied using the wings of the fruit fly Drosophila melanogaster as a model system[7,8] Both robustness and developmental stability have been considered to be polygenic traits whose variation is primarily determined by many genes with small impacts, instead of by few genes with substantial impacts[9,10]. In Drosophila, aerobic glycolysis is indispensable for body growth during larval development[17,18], suggesting that glycemic control is a central component for the maintenance of developmental integrity by providing a constant supply of energy to each organ

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