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.

FIG. 1.—

The mitochondrial genome of Nasonia. Linearized map showing gene order in the 2 fragments of the Nasonia mtDNA. The complete mitochondrial genome of the honeybee Apis mellifera (GenBank accession number L06178) is shown for comparison. A large inversion encompassing 6 protein-coding genes and 4 tRNAs is highlighted. Asterisks indicate other rearrangements in gene order, including the position of nad2. Unknown junctions are indicated with a question mark. See text for details.

FIG. 2.—

Pairwise comparison of sequence divergence for each mitochondrial gene. Genes are ordered according to their position in the mitochondrial genome of Nasonia. The mtDNA sequences of Nasonia vitripennis (NV) strain AsymC was used for between-species calculation; Nasonia vitripennis × Nasonia vitripennis compares AsymC and HiCD12 strains of N. vitripennis. Values of Ks and Ka are corrected by the JC method. Similar statistics for Drosophila melanogaster (DM; U37541) and Drosophila simulans (DS; AF200833) is shown for comparison.

FIG. 3.—

(A) Consensus tree of the 6 most parsimonious trees for the combined mitochondrial sequences—total of 2,256 aligned nucleotides, 506 parsimony-informative characters, tree length = 988, consistency index = 0.7581, and retention index = 0.9652. Bootstrap support is shown for relevant braches, Jackknife support (with 33% deletion) was also estimated and it was always 100% for the same branches (data not shown). (B) Amino acid replacements for each of the 3 studied genes were placed in the trees braches under a most parsimonious framework. Tickers bars are unambiguous changes, and lighter bars are replacements for which the polarity of the change could not be determined. Brach length is proportional to all possible changes.

FIG. 4.—

The process of Compensation-Draft Feedback is shown. Fixation of a mildly deleterious mutation favors compensatory mutations, which in turn can result in fixation of new mildly deleterious mutations by genetic draft (hitchhiking of harmful mutations in the nonrecombining mitochondrial genome). The process can be started initially by selection for a beneficial mutation, increase by drift of a mildly deleterious mutation, or selective sweeps due to associated cytoplasmically inherited microorganisms such as Wolbachia. Higher mitochondrial mutation rates will accelerate the process.