Mitochondrial-Nuclear Epistasis Affects Fitness Within Species but Does Not Contribute to Fixed Incompatibilities Between Species of Drosophila

Abstract

Efficient mitochondrial function requires physical interactions between the proteins encoded by the mitochondrial and nuclear genomes. Co-evolution between these genomes may result in the accumulation of incompatibilities between divergent lineages. We test whether mitochondrialnuclear incompatibilities have accumulated within the Drosophila melanogaster species subgroup by combining divergent mitochondrial and nuclear lineages and quantifying the effects on relative fitness. Precise placement of nine mtDNAs from D. melanogaster, D. simulans and D. mauritiana into two D. melanogaster nuclear genetic backgrounds reveals significant mitochondrial-nuclear epistasis affecting fitness in females. Combining the mitochondrial genomes with three different D. melanogaster X chromosomes reveals significant epistasis for male fitness between X-linked and mitochondrial variation. However, we find no evidence that the more than 500 fixed differences between the mitochondrial genomes of D. melanogaster and the D. simulans species complex are incompatible with the D. melanogaster nuclear genome. Rather, the interactions of largest effect occur between mitochondrial and nuclear polymorphisms that segregate within species of the D. melanogaster species subgroup. We propose that a low mitochondrial substitution rate, resulting from a low mutation rate and/or efficient purifying selection, precludes the accumulation of mitochondrial-nuclear incompatibilities among these Drosophila species.

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

“…These parallel observations of organismal traits and gene modulations conferred by the Y chromosome and mitochondria might point to a regulatory network of spermatogenesis, including both parties and other nuclear genes. We expect that mitochondria-X chromosome interactions (Rand et al, 2001;Montooth et al, 2010) and mitochondria-Y chromosome interactions may turn out to be critically important in spermatogenesis. Finally, genes specific to the accessory glands were downregulated in males with resistant Y chromosomes, suggesting that this particular tissue might provide protection for spermatogenesis in a stressful environment (that is, sex ratio distortion).…”

Mitochondrial-Nuclear Epistasis Contributes to Phenotypic Variation and Coadaptation in Natural Isolates of Saccharomyces cerevisiae

“…Introgression of mtDNAs from Drosophila simulans to D. melanogaster had significant effects on respiratory complexes (Sackton et al 2003), development (Montooth et al 2010), and aging (Rand et al 2006). Disrupted oxidative phosphorylation pathways were observed in F 2 male hybrids of Nasonia wasps (Ellison et al 2008;Niehuis et al 2008;Koevoets et al 2012a).…”

“…Interspecific mt-n incompatibilities between yeasts in the Saccharomyces sensu stricto genus can lead to complete respiratory deficiencies (Sulo et al 2003;Lee et al 2008;Chou et al 2010; but see Prochazka et al 2012). While incompatibilities between species generally leads to a decline in fitness, mt-n incompatibilities do not always tightly align with genetic distance; larger epistatic responses to mtDNA exchanges were observed within D. melanogaster populations than between species (Montooth et al 2010). The Dobzhansky-Muller-type mt-n incompatibilities that sometimes exist between species may have contributed to speciation events (Trier et al 2014;Wolff et al 2014), although the dynamics of mt-n coevolution are not well enough understood to make substantial conclusions.…”

“…These interactions have been shown to have direct consequences on healthrelated and life-history phenotypes in several taxa. In insects such as Drosophila and Callosobruchus (seed beetle), exchanging mtDNA variants between distinct populations has led to lowered metabolic rate (Arnqvist et al 2010), decreased egg-to-adult survival (Dowling et al 2007a;Montooth et al 2010), and shortened life span (Clancy 2008;Zhu et al 2014). Interpopulation hybrids of the marine copepod Tigriopus suffered compromised oxidative phosphorylation (OXPHOS) capacities Burton 2006, 2008b) and reduced mitochondrial transcription (Ellison and Burton 2008a), most likely influenced by interactions between alleles of the nuclearencoded RNA polymerase and mtDNA variants (Ellison and Burton 2010).…”

Explaining Darwin’s Corollary to Haldane’s Rule: The Role of Mitonuclear Interactions in Asymmetric Postzygotic Isolation Among Toads

“…If the proportion of mitochondrial to nuclear substitutions in lineage A exceeds that in lineage B, we expect more mitonuclear DMIs in AB F 1 hybrids with A mothers vs. BA hybrids with B mothers, simply because there are more potential incompatibilities in the AB cross than in the BA cross. Thus, if mitonuclear DMIs contribute significantly to lowered interpopulation (Burton et al 2006;Ellison and Burton 2008;Montooth et al 2010;Meiklejohn et al 2013) or interspecific (e.g., Fishman and Willis 2006;Lee et al 2008;Rieseberg and Blackman 2010) fitness, as often argued (e.g., Rand et al 2004;Gershoni et al 2009;Lane 2011;Burton and Barreto 2012), directional asymmetry may be predictable from relative rates of mitochondrial vs. nuclear evolution. Turelli and Moyle (2007) conjectured that the deterministic signal associated with directional effects produced by a particular class of DMIs (e.g., mitonuclear incompatibilities) was likely to be overwhelmed by both stochastic effects and other classes of asymmetric incompatibilities.…”