Contrasting patterns of selective constraints in nuclear-encoded genes of the oxidative phosphorylation pathway in holometabolous insects and their possible role in hybrid breakdown in Nasonia

Abstract

The principal energy generating system in animals is the oxidative phosphorylation (OXPHOS) pathway, which depends on the tight interaction of nuclear and mitochondrial encoded genes to function properly. Mitochondrial genes accumulate substitutions more quickly than nuclear genes, yet the impact of selection on mitochondrial genes is significantly reduced relative to nuclear genes due to the non-recombining nature of the mitochondrial genome and its predicted smaller effective population size. It has therefore been hypothesized that the nuclear encoded genes of the OXPHOS pathway are under strong selective pressure to compensate for the accumulation of deleterious nucleotide substitutions in mitochondrial encoded OXPHOS genes; a process known as compensatory co-adaptation. We evaluated this hypothesis by analyzing nuclear encoded OXPHOS genes for signatures of positive selection as well as evolutionary constraints at amino acid sites. We considered OXPHOS genes of six holometabolous insects and their orthologs from three Nasonia parasitoid wasps; hybrids of which suffer from an increased mortality rate caused by cytonuclear genic incompatibilities. Although nuclear OXPHOS genes are typically highly conserved, we found significant evidence for elevated amino acid divergence in four of the 59 studied nuclear encoded OXPHOS genes. We also found that three of these four genes, as well as six other OXPHOS genes, contain amino acid substitutions between Nasonia species at evolutionarily constrained sites. It is possible that these genes account for the reported incompatibility in Nasonia hybrids and their characterization may lead to a better understanding of the role of positive selection in the genetics of speciation.

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

“…Nasonia has a mitochondrial substitution rate that is 30 times higher than the nuclear substitution rate (Oliveira et al 2008). This substitution rate is hypothesized to have driven evolution of the nuclear‐encoded genes of the oxidative phosphorylation pathway and the accumulation of mitochondrial–nuclear incompatibilities among Nasonia species that decrease hybrid fitness (Oliveira et al 2008; Gibson et al 2010; The Nasonia Genome Working Group 2010). Third, populations of the marine copepod T. californicus have mitochondrial substitution rates that are 25‐fold higher than nuclear rates and experience mitochondrial–nuclear incompatibilities that decrease hybrid fitness (Burton et al 2006; Ellison and Burton 2008a).…”

Temperature stress increases hybrid incompatibilities in the parasitic wasp genus Nasonia

“…Most distorted genomic regions identified here encompass at least one OXPHOS gene that codes for a protein that differs between N. vitripennis and N. longicornis (black arrows in Fig. 4, after Gibson et al. , 2010).…”

The dynamics of mito-nuclear coevolution: A perspective from bivalve species with two different mechanisms of mitochondrial inheritance

“…For instance, the rate of amino acid sequence evolution of mitochondrial subunits is remarkably lower than that of nuclear subunits in most previously investigated taxa (see, for example, Nabholz, Ellegren, & Wolf, ; Popadin, Nikolaev, Junier, Baranova, & Antonarakis, ). Accordingly, there is evidence for strong purifying selection acting on mitochondrially encoded OXPHOS subunits (Piganeau & Eyre‐Walker, ; Popadin et al., ), even if signs of positive selection were also reported (Castellana, Vicario, & Saccone, ; Gibson, Niehuis, Verrelli, & Gadau, ; James, Piganeau, & Eyre‐Walker, ; Pavlova et al., ).…”