Abstract

The genetics of phenotypic responses to changing environments remains elusive. Using whole-genome quantitative gene expression as a model, here we study how the genetic architecture of regulatory variation in gene expression changed in a population of fully sequenced inbred Drosophila melanogaster strains when flies developed in different environments (25 °C and 18 °C). We find a substantial fraction of the transcriptome exhibited genotype by environment interaction, implicating environmentally plastic genetic architecture of gene expression. Genetic variance in expression increases at 18 °C relative to 25 °C for most genes that have a change in genetic variance. Although the majority of expression quantitative trait loci (eQTLs) for the gene expression traits in the two environments are shared and have similar effects, analysis of the environment-specific eQTLs reveals enrichment of binding sites for two transcription factors. Finally, although genotype by environment interaction in gene expression could potentially disrupt genetic networks, the co-expression networks are highly conserved across environments. Genes with higher network connectivity are under stronger stabilizing selection, suggesting that stabilizing selection on expression plays an important role in promoting network robustness.

Highlights

  • The genetics of phenotypic responses to changing environments remains elusive

  • Using a simple but powerful design, we provided a comprehensive characterization of the response of the regulatory genetic variation of the Drosophila transcriptome to environmental change

  • This was instrumental in partitioning the variance in gene expression and providing a global characterization of the extent of genetic canalization or decanalization and genotype by environment interaction (G×E)

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Summary

Introduction

The genetics of phenotypic responses to changing environments remains elusive. Using whole-genome quantitative gene expression as a model, here we study how the genetic architecture of regulatory variation in gene expression changed in a population of fully sequenced inbred Drosophila melanogaster strains when flies developed in different environments (25 °C and 18 °C). We find a substantial fraction of the transcriptome exhibited genotype by environment interaction, implicating environmentally plastic genetic architecture of gene expression. Organisms living in fluctuating environments or entering novel environments must possess mechanisms to cope with environmental changes. One such mechanism is to change expressed phenotypes in response to different environments, a phenomenon called phenotypic plasticity[1]. In addition to environmental factors, phenotypes can respond to genetic perturbations in a plastic or homeostatic manner, which characterizes the potential of an organism to express phenotypes when genes mutate. Describes the change from a homeostatic state to a plastic one, which allows phenotypic expression of genetic and/or environmental variation[4,5]. G×E is of paramount importance to realize personalized medicine such as individualized drug therapy[12]

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