Abstract

BackgroundMito-nuclear gene interactions regulate energy conversion, and are fundamental to eukaryotes. Generally, mito-nuclear coadaptation would be most efficient if the interacting nuclear genes were X-linked, because this maximizes the probability of favorable mito-nuclear allelic combinations co-transmitting across generations. Thus, under a coadaptation (CA) hypothesis, nuclear genes essential for mitochondrial function might be under selection to relocate to the X-chromosome. However, maternal inheritance predisposes the mitochondrial DNA (mtDNA) to accumulate variation that, while male-harming, is benign to females. Numerous nuclear genes were recently reported in Drosophila melanogaster, which exhibit male-specific patterns of differential expression when placed alongside different mtDNA haplotypes, suggesting that nuclear genes are sensitive to an underlying male-specific mitochondrial mutation load. These genes are thus candidates for involvement in mito-nuclear interactions driven by sexual conflict (SC), and selection might have moved them off the X-chromosome to facilitate an optimal evolutionary counter-response, through males, to the presence of male-harming mtDNA mutations. Furthermore, the presence of male-harming mtDNA mutations could exert selection for modifiers on the Y-chromosome, thus placing these mito-sensitive nuclear genes at the center of an evolutionary tug-of-war between mitochondrion and Y-chromosome.We test these hypotheses by examining the chromosomal distributions of three distinct sets of mitochondrial-interacting nuclear genes in D. melanogaster; the first is a list of genes with mitochondrial annotations by Gene Ontologies, the second is a list comprising the core evolutionary-conserved mitochondrial proteome, and the third is a list of genes involved in male-specific responses to maternally-inherited mitochondrial variation and which might be putative targets of Y-chromosomal regulation.ResultsGenes with mitochondrial annotations and genes representing the mitochondrial proteome do not exhibit statistically-significant biases in chromosomal representation. However, genes exhibiting sex-specific sensitivity to mtDNA are under-represented on the X-chromosome, over-represented among genes known to be sensitive to Y-chromosomal variation, and among genes previously associated with male fitness, but under-represented among genes associated with direct sexual antagonism.ConclusionsOur results are consistent with the SC hypothesis, suggesting that mitochondrial mutational pressure selects for gene movement off-the-X, hence enabling mito-nuclear coadaptation to proceed along trajectories that result in optimized fitness in both sexes.

Highlights

  • Mito-nuclear gene interactions regulate energy conversion, and are fundamental to eukaryotes

  • The products of mito-nuclear interactions are so vital to life, that traditionally it was thought that any genetic variation accumulating in the coding regions of the mitochondrial DNA (mtDNA) should be deleterious to function and purified by selection, and that the mitochondria should contain little genetic variation of evolutionary relevance [3,4]

  • We have shown that the nuclear genes that are sensitive to cryptic mtDNA polymorphism, and whose expression is modified in males but not in females, overlap significantly with those genes that are sensitive to cryptic Y-chromosome polymorphisms in males

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Summary

Introduction

Mito-nuclear gene interactions regulate energy conversion, and are fundamental to eukaryotes. Over the past two decades, a large body of empirical evidence has accumulated that shows that natural levels of mitochondrial allelic variance contribute to phenotypic variation in the expression of evolutionarily important traits [5,6], such as metabolism [7], life span and ageing [8,9,10], reproductive fitness [11,12], viability [13,14] and gene expression [15] These findings have prompted a re-evaluation of the role of the mitochondrial genome in driving fundamental evolutionary processes [6,16,17], including the evolution of genome organization [18]. This is the coadapted (CA) mito-nuclear hypothesis, and it predicts that nuclear genes involved in mito-nuclear interactions that encode important mitochondrial functions, should be enriched on the X-chromosome

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