Animal mitochondria, positive selection and cyto-nuclear coevolution: insights from pulmonates

PLoS One. 2013 Apr 19;8(4):e61970. doi: 10.1371/journal.pone.0061970. Print 2013.


Pulmonate snails have remarkably high levels of mtDNA polymorphism within species and divergence between species, making them an interesting group for the study of mutation and selection on mitochondrial genomes. The availability of sequence data from most major lineages - collected largely for studies of phylogeography - provides an opportunity to perform several tests of selection that may provide general insights into the evolutionary forces that have produced this unusual pattern. Several protein coding mtDNA datasets of pulmonates were analyzed towards this direction. Two different methods for the detection of positive selection were used, one based on phylogeny, and the other on the McDonald-Kreitman test. The cyto-nuclear coevolution hypothesis, often implicated to account for the high levels of mtDNA divergence of some organisms, was also addressed by assessing the divergence pattern exhibited by a nuclear gene. The McDonald-Kreitman test indicated multiple signs of positive selection in the mtDNA genes, but was significantly biased when sequence divergence was high. The phylogenetic method identified five mtDNA datasets as affected by positive selection. In the nuclear gene, the McDonald-Kreitman test provided no significant results, whereas the phylogenetic method identified positive selection as likely present. Overall, our findings indicate that: 1) slim support for the cyto-nuclear coevolution hypothesis is present, 2) the elevated rates of mtDNA polymorphims and divergence in pulmonates do not appear to be due to pervasive positive selection, 3) more stringent tests show that spurious positive selection is uncovered when distant taxa are compared and 4) there are significant examples of positive selection acting in some cases, so it appears that mtDNA evolution in pulmonates can escape from strict deleterious evolution suggested by the Muller's ratchet effect.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Base Sequence
  • Cell Nucleus / genetics*
  • Cytochromes c / genetics
  • DNA, Mitochondrial
  • Evolution, Molecular*
  • Genetic Variation
  • Likelihood Functions
  • Mitochondria / genetics*
  • Mutation / genetics
  • Selection, Genetic*
  • Snails / genetics*
  • Species Specificity


  • DNA, Mitochondrial
  • Cytochromes c

Grant support

This project was partially funded by the “John S. Latsis” Public Benefit Foundation, and the sole responsibility for the content lies with its authors. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. No additional external funding was received for this study.