Rapidly Evolving Mitochondrial Genome and Directional Selection in Mitochondrial Genes in the Parasitic Wasp Nasonia (Hymenoptera: Pteromalidae)

Abstract

We sequenced the nearly complete mtDNA of 3 species of parasitic wasps, Nasonia vitripennis (2 strains), Nasonia giraulti, and Nasonia longicornis, including all 13 protein-coding genes and the 2 rRNAs, and found unusual patterns of mitochondrial evolution. The Nasonia mtDNA has a unique gene order compared with other insect mtDNAs due to multiple rearrangements. The mtDNAs of these wasps also show nucleotide substitution rates over 30 times faster than nuclear protein-coding genes, indicating among the highest substitution rates found in animal mitochondria (normally <10 times faster). A McDonald and Kreitman test shows that the between-species frequency of fixed replacement sites relative to silent sites is significantly higher compared with within-species polymorphisms in 2 mitochondrial genes of Nasonia, atp6 and atp8, indicating directional selection. Consistent with this interpretation, the Ka/Ks (nonsynonymous/synonymous substitution rates) ratios are higher between species than within species. In contrast, cox1 shows a signature of purifying selection for amino acid sequence conservation, although rates of amino acid substitutions are still higher than for comparable insects. The mitochondrial-encoded polypeptides atp6 and atp8 both occur in F0F1ATP synthase of the electron transport chain. Because malfunction in this fundamental protein severely affects fitness, we suggest that the accelerated accumulation of replacements is due to beneficial mutations necessary to compensate mild-deleterious mutations fixed by random genetic drift or Wolbachia sweeps in the fast evolving mitochondria of Nasonia. We further propose that relatively high rates of amino acid substitution in some mitochondrial genes can be driven by a "Compensation-Draft Feedback"; increased fixation of mildly deleterious mutations results in selection for compensatory mutations, which lead to fixation of additional deleterious mutations in nonrecombining mitochondrial genomes, thus accelerating the process of amino acid substitutions.

Distinguishing the effects of selection from demographic history in the genetic variation of two sister passerines based on mitochondrial–nuclear comparison

“…Additional studies on mechanistic links between phenotypic or physiological changes and genetic substitutions and consequent ecological interactions are warranted. Despite the plausible evidence found here supporting positive selection directly targeting the mtDNA ND2 gene, alternative hypotheses such as mitochondrialnuclear coadaptation (Gershnoi et al, 2009) and selective sweeps caused by linkage to either other mtDNA genes (Oliveira et al, 2007) or the W chromosome due to shared segregation process (Berlin et al, 2007) are worthy of further investigation.…”

Comparative mitochondrial genomic analyses of three chemosynthetic vesicomyid clams from deep‐sea habitats

“…Malfunctions of these PCGs would be lethal or at least severely affect fitness. Lethal mutation will be excluded, while neutral, mildly deleterious or suited mutation will be retained (Oliveira et al., 2008). Vesicomyid species usually reside in pore water that contains high concentration of toxic chemicals such as hydrogen sulfide and heavy metal, and symbioses with chemosynthetic bacteria.…”

“…In addition, one extensive noncoding “A + T‐rich” region is usually present which is known to contain elements controlling the initiation of replication and transcription (Boore, 1999; Wolstenholme, 1992). Due to their fundamental roles in oxidative phosphorylation responsible for energy production (Saraste, 1999), mt PCGs are generally thought to evolve primarily under constant purifying selection (Oliveira, Raychoudhury, Lavrov, & Werren, 2008). During the past decade, mt genomes had been intensively investigated for the study of molecular evolution, population genetics, and inferring phylogeny (Boore, 1999; Shen et al., 2017).…”

Nucleotide Polymorphism and Within-Gene Recombination in Daphnia magna and D. pulex, Two Cyclical Parthenogens

“…As for our estimates, multiple assumptions were necessary, most notably a constant mitochondrial rate (per year) of nucleotide substitution among animals. Yet, even among mammals this rate can vary by two orders of magnitude (Nabholz et al 2008) and it is also highly variable among insects (Oliveira et al 2008). If substitution rates were higher than assumed, this may have led to an overestimation of divergence time.…”

“…Additionally, polymorphism in the ancestral species could contribute to a potential overestimation of divergence times if the two daughter species received highly divergent copies (Lynch and Jarrell 1993). Finally, because of the linkage of the whole mitochondrial genome, background selection and hitchhiking potentially contribute further difficulties in the interpretation of mitochondrial divergence times (Bazin et al 2006;Oliveira et al 2008). Until the relevant data are available for Daphnia, the discrepant divergence time estimates cannot currently be fully explained.…”