Abstract

The mitonuclear genome is the most successful co-evolved mutualism in the history of life on Earth. The cross-talk between the mitochondrial and nuclear genomes has been shaped by conflict and cooperation for more than 1.5 billion years, yet this system has adapted to countless genomic reorganizations by each partner, and done so under changing environments that have placed dramatic biochemical and physiological pressures on evolving lineages. From putative anaerobic origins, mitochondria emerged as the defining aerobic organelle. During this transition, the two genomes resolved rules for sex determination and transmission that made uniparental inheritance the dominant, but not a universal pattern. Mitochondria are much more than energy-producing organelles and play crucial roles in nutrient and stress signalling that can alter how nuclear genes are expressed as phenotypes. All of these interactions are examples of genotype-by-environment (GxE) interactions, gene-by-gene (GxG) interactions (epistasis) or more generally context-dependent effects on the link between genotype and phenotype. We provide evidence from our own studies in Drosophila, and from those of other systems, that mitonuclear interactions—either conflicting or cooperative—are common features of GxE and GxG. We argue that mitonuclear interactions are an important model for how to better understand the pervasive context-dependent effects underlying the architecture of complex phenotypes. Future research in this area should focus on the quantitative genetic concept of effect size to place mitochondrial links to phenotype in a proper context.This article is part of the theme issue ‘Linking the mitochondrial genotype to phenotype: a complex endeavour’.

Highlights

  • Mitochondria influence most phenotypes in all eukaryotes

  • We propose the most important role that mitochondria play in linking genotype to phenotype is through their context-dependent epistatic and GxE interactions with the nucleus and the environment

  • We argue that mitonuclear genetic variation embodies highly complex and pervasive GxG and GxE interactions that modify organismal fitness and function in non-additive ways and is an ideal context for evaluating the nature of the polygenic and omnigenic models

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Summary

Introduction

Mitochondria influence most phenotypes in all eukaryotes. This may be true for other subcellular structures like ribosomes, the endoplasmic reticulum or centrioles, but mitochondria are so much more interesting because they have their own polyploid genome that is distributed across the cytoplasm and is distinct from the nuclear genome. It is our opinion that experimental studies demonstrating mtDNA phenotype effects in one or two nuclear backgrounds or environmental contexts by no means establish that this pattern is general in the natural world This is an old and thorny problem in the experimental population and ecological genetics. We argue that mitonuclear genetic variation embodies highly complex and pervasive GxG and GxE interactions that modify organismal fitness and function in non-additive ways and is an ideal context for evaluating the nature of the polygenic and omnigenic models This view has been informed by empirical studies in the fruit fly Drosophila melanogaster and other model organisms and follows from the enormity of functions in eukaryotic cells that are governed by mitonuclear crosstalk [50,51]. To claim that mtDNA is more important than the entire nuclear genome as a driver of organismal fitness and adaptation does not seem warranted by these data

Nonlinear interactions: complications for phenotypic prediction
Experimental approaches to map mitochondrial genotypes to phenotypes
Phenotypic repeatability is crucial
Conflict and cooperation—negative and positive effects by another name
Findings
Concluding remarks
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