Abstract
Genetic effects are often context dependent, with the same genotype differentially affecting phenotypes across environments, life stages, and sexes. We used an environmental manipulation designed to increase energy demand during development to investigate energy demand as a general physiological explanation for context‐dependent effects of mutations, particularly for those mutations that affect metabolism. We found that increasing the photoperiod during which Drosophila larvae are active during development phenocopies a temperature‐dependent developmental delay in a mitochondrial‐nuclear genotype with disrupted metabolism. This result indicates that the context‐dependent fitness effects of this genotype are not specific to the effects of temperature and may generally result from variation in energy demand. The effects of this genotype also differ across life stages and between the sexes. The mitochondrial‐nuclear genetic interaction disrupts metabolic rate in growing larvae, but not in adults, and compromises female, but not male, reproductive fitness. These patterns are consistent with a model where context‐dependent genotype‐phenotype relationships may generally arise from differences in energy demand experienced by individuals across environments, life stages, and sexes.
Highlights
Genetic effects on traits are often context dependent, such that a genotype that improves fitness under one context may have no effect or even a deleterious effect in another context
We show that the magnitude of fitness effects of this genetic interaction correlates positively with the degree of energy demand among developmental treatments that accelerate growth rate, across developmental stages that differ in the cost of growth, and between sexes with potentially different costs of reproduction
Because natural selection acts upon the subset of expressed genetic variation that affects fitness, the fate of new mutations may depend on the landscape of genetic backgrounds and environments experienced by a population (e.g., Remold and Lenski 2004; Chandler et al 2013; Lachance et al 2013; Wang et al 2013; Kammenga, 2017)
Summary
Genetic effects on traits are often context dependent, such that a genotype that improves fitness under one context may have no effect or even a deleterious effect in another context. We show that the magnitude of fitness effects of this genetic interaction correlates positively with the degree of energy demand among developmental treatments that accelerate growth rate, across developmental stages that differ in the cost of growth, and between sexes with potentially different costs of reproduction These internal and external contexts create variable demands on energy metabolism that will impact the efficacy of natural selection acting on metabolic mutations in populations. If the relationship between genotype and fitness is generally conditional on internal or external environmental factors (i.e., is context dependent), elucidating general principles underlying genotype-phenotype–environment interactions is critical for understanding evolutionary processes such as the maintenance of genetic variation for life-history traits (Roff and Fairbairn 2007; Van Dyken and Wade 2010; Mackay 2014). While many good examples of the importance of environmental context for tradeoffs exist (reviewed in Asplen et al 2012), understanding the genetic architecture underlying tradeoffs and the physiological mechanisms mediating them lags behind (Roff and Fairbairn 2007)
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