Analyses of Nuclearly Encoded Mitochondrial Genes Suggest Gene Duplication as a Mechanism for Resolving Intralocus Sexually Antagonistic Conflict in Drosophila

Abstract

Gene duplication is probably the most important mechanism for generating new gene functions. However, gene duplication has been overlooked as a potentially effective way to resolve genetic conflicts. Here, we analyze the entire set of Drosophila melanogaster nuclearly encoded mitochondrial duplicate genes and show that both RNA- and DNA-mediated mitochondrial gene duplications exhibit an unexpectedly high rate of relocation (change in location between parental and duplicated gene) as well as an extreme tendency to avoid the X chromosome. These trends are likely related to our observation that relocated genes tend to have testis-specific expression. We also infer that these trends hold across the entire Drosophila genus. Importantly, analyses of gene ontology and functional interaction networks show that there is an overrepresentation of energy production-related functions in these mitochondrial duplicates. We discuss different hypotheses to explain our results and conclude that our findings substantiate the hypothesis that gene duplication for male germline function is likely a mechanism to resolve intralocus sexually antagonistic conflicts that we propose are common in testis. In the case of nuclearly encoded mitochondrial duplicates, our hypothesis is that past sexually antagonistic conflict related to mitochondrial energy function in Drosophila was resolved by gene duplication.

The Resolution of Sexual Antagonism by Gene Duplication

“…Data from Drosophila and mammals indicate that there is a good deal of duplicate gene traffic between the sex chromosomes and autosomes, with male functions (male-and testis-biased expression) preferentially associated with derived Y-linked and autosomal duplicates (Betrán et al 2002;Skaletsky et al 2003;Emerson et al 2004;Meisel et al 2009;Vibranovski et al 2009b;Gallach et al 2010). These patterns are consistent with predictions of the theory of sexual antagonism.…”

Mitonuclear interactions: evolutionary consequences over multiple biological scales

“…Second, many species possess duplicates of nuclear-encoded mitochondrial genes, which exhibit tissue-specific (generally testis) expression. In one study on fruit flies, the expression of some mitochondrial gene duplicates was exclusively limited to testes and the expression of these duplicates outweighed the expression of the original parental genes threefold in the testes, whereas in all other tissues, gene duplicates were not expressed at all, instead fully relying on the expression of the parental variant [97].…”

“…The presence of heteroplasmy in mtDNA, coupled with such context-dependence in expression of alternative mitochondrial gene isoforms, thus provides explicit scope for tissue-dependent intraindividual mitonuclear interactions, [97]. The existence of differential tissue-specific or physiologically induced expression of genes means that different combinations of mitochondrial components-with different catalytic properties-are expressed and assembled in different tissues or in response to particular stimuli.…”

Natural variation of the Y chromosome suppresses sex ratio distortion and modulates testis-specific gene expression in Drosophila simulans

“…Intragenomic conflicts over sex ratio control, which is a perpetual tug-of-war among the X, the Y, the autosomes and the cytoplasmic genes, might cause several well-known genomic patterns uncovered in recent years, including meiotic sex chromosome inactivation and out-of-the-X traffic of testis-specific genes (Meiklejohn and Tao, 2010). Interestingly, many of the mitochondrial genes have evolved to function specifically during spermatogenesis in Drosophila (Gallach et al, 2010). This organelle has an essential role in sperm morphogenesis (Noguchi et al, 2011) and motility (Fuller, 1993), although it is not inherited through males in Drosophila (DeLuca and O'Farrell, 2012).…”