MBE Advance Access published online on July 24, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn159
Research Article |
Rapidly Evolving Mitochondrial Genome and Directional Selection in Mitochondrial Genes in the Parasitic Wasp Nasonia (Hymenoptera: Pteromalidae)
1 Department of Biology, University of Rochester, Rochester, NY 14627, USA
2 Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA 50011, USA
* Corresponding author / present address: Deodoro C. S. G. Oliveira; Departament de Genètica i de Microbiologia, Universitat Autònoma de Barcelona, Bellaterra, BCN 08193, Spain; Telephone number: +34 93 581 2719; Fax number: +34 93 581 2387; e-mail: Deodoro.Oliveira{at}uab.cat
Received for publication December 20, 2007. Revision received June 24, 2008. Accepted for publication July 19, 2008.
We sequenced the nearly complete mtDNA of three species of parasitic wasps, Nasonia vitripennis (two strains), N. giraulti, and N. longicornis, including all 13 protein-coding genes and the two rRNAs, and found unusual patterns of mitochondrial evolution. The Nasonia mtDNA has a unique gene order compared to 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 to within-species polymorphisms in two mitochondrial genes of Nasonia, atp6 and atp8, indicating directional selection. Consistent with this interpretation, the Ka/Ks (non-synonymous/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. Since 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 non-recombining mitochondrial genomes, thus accelerating the process of amino acid substitutions.
Key Words: Nasonia • mitochondrial genome • gene organization • rates of evolution