Skip to main content
Genetics logoLink to Genetics
. 1996 Jul;143(3):1349–1357. doi: 10.1093/genetics/143.3.1349

Degree of Selective Constraint as an Explanation of the Different Rates of Evolution of Gender-Specific Mitochondrial DNA Lineages in the Mussel Mytilus

D T Stewart 1, E R Kenchington 1, R K Singh 1, E Zouros 1
PMCID: PMC1207403  PMID: 8807306

Abstract

Mussels of the genus Mytilus segregate for a maternally transmitted F lineage and a paternally transmitted M lineage of mitochondrial DNA. Previous studies demonstrated that these lineages are older than the species of the M. edulis complex and that the M lineage evolves faster than the F lineage. Here we show that the latter observation also applies to a region of the molecule with no assigned function. Sequence data for the mitochondrial COIII gene and the ``unassigned'' region of the F and M lineages of M. edulis and M. trossulus are used to evaluate various hypotheses that may account for the faster rate of evolution of the M lineage. Tests based on the proportion of synonymous and nonsynonymous substitutions suggest that the M lineage experiences relatively relaxed selection. Further support for this hypothesis comes from an examination of COIII amino acid substitutions at sites defined as either conserved or variable based on the pattern of variation in other mollusks and Drosophila. Most substitutions in the M lineage occur in regions that are also variable among non-Mytilus taxa. We suggest that these differences in selection pressure are a consequence of doubly uniparental mitochondrial DNA transmission in Mytilus.

Full Text

The Full Text of this article is available as a PDF (886.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Barriga Sosa I. A., Beckenbach K., Hartwick B., Smith M. J. The molecular phylogeny of five eastern north Pacific octopus species. Mol Phylogenet Evol. 1995 Jun;4(2):163–174. doi: 10.1006/mpev.1995.1016. [DOI] [PubMed] [Google Scholar]
  2. Boore J. L., Brown W. M. Complete DNA sequence of the mitochondrial genome of the black chiton, Katharina tunicata. Genetics. 1994 Oct;138(2):423–443. doi: 10.1093/genetics/138.2.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Clary D. O., Wolstenholme D. R. The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol. 1985;22(3):252–271. doi: 10.1007/BF02099755. [DOI] [PubMed] [Google Scholar]
  4. Hatzoglou E., Rodakis G. C., Lecanidou R. Complete sequence and gene organization of the mitochondrial genome of the land snail Albinaria coerulea. Genetics. 1995 Aug;140(4):1353–1366. doi: 10.1093/genetics/140.4.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Hoeh W. R., Blakley K. H., Brown W. M. Heteroplasmy suggests limited biparental inheritance of Mytilus mitochondrial DNA. Science. 1991 Mar 22;251(5000):1488–1490. doi: 10.1126/science.1672472. [DOI] [PubMed] [Google Scholar]
  6. Hoffmann R. J., Boore J. L., Brown W. M. A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics. 1992 Jun;131(2):397–412. doi: 10.1093/genetics/131.2.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hudson R. R. How can the low levels of DNA sequence variation in regions of the drosophila genome with low recombination rates be explained? Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6815–6818. doi: 10.1073/pnas.91.15.6815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hurst L. D., Hoekstra R. F. Evolutionary genetics. Shellfish genes kept in line. Nature. 1994 Apr 28;368(6474):811–812. doi: 10.1038/368811a0. [DOI] [PubMed] [Google Scholar]
  9. Longo F. J., Dornfeld E. J. The fine structure of spermatid differentiation in the mussel, Mytilus edulis. J Ultrastruct Res. 1967 Oct 31;20(5):462–480. doi: 10.1016/s0022-5320(67)80113-8. [DOI] [PubMed] [Google Scholar]
  10. McDonald J. H., Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. doi: 10.1038/351652a0. [DOI] [PubMed] [Google Scholar]
  11. Nachman M. W., Boyer S. N., Aquadro C. F. Nonneutral evolution at the mitochondrial NADH dehydrogenase subunit 3 gene in mice. Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6364–6368. doi: 10.1073/pnas.91.14.6364. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Rand D. M., Dorfsman M., Kann L. M. Neutral and non-neutral evolution of Drosophila mitochondrial DNA. Genetics. 1994 Nov;138(3):741–756. doi: 10.1093/genetics/138.3.741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Rawson P. D., Hilbish T. J. Evolutionary relationships among the male and female mitochondrial DNA lineages in the Mytilus edulis species complex. Mol Biol Evol. 1995 Sep;12(5):893–901. doi: 10.1093/oxfordjournals.molbev.a040266. [DOI] [PubMed] [Google Scholar]
  14. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  15. Skibinski D. O., Gallagher C., Beynon C. M. Mitochondrial DNA inheritance. Nature. 1994 Apr 28;368(6474):817–818. doi: 10.1038/368817b0. [DOI] [PubMed] [Google Scholar]
  16. Skibinski D. O., Gallagher C., Beynon C. M. Sex-limited mitochondrial DNA transmission in the marine mussel Mytilus edulis. Genetics. 1994 Nov;138(3):801–809. doi: 10.1093/genetics/138.3.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Stewart D. T., Saavedra C., Stanwood R. R., Ball A. O., Zouros E. Male and female mitochondrial DNA lineages in the blue mussel (Mytilus edulis) species group. Mol Biol Evol. 1995 Sep;12(5):735–747. doi: 10.1093/oxfordjournals.molbev.a040252. [DOI] [PubMed] [Google Scholar]
  18. Zouros E., Ball A. O., Saavedra C., Freeman K. R. Mitochondrial DNA inheritance. Nature. 1994 Apr 28;368(6474):818–818. doi: 10.1038/368818a0. [DOI] [PubMed] [Google Scholar]
  19. Zouros E., Freeman K. R., Ball A. O., Pogson G. H. Direct evidence for extensive paternal mitochondrial DNA inheritance in the marine mussel Mytilus. Nature. 1992 Oct 1;359(6394):412–414. doi: 10.1038/359412a0. [DOI] [PubMed] [Google Scholar]
  20. Zuker M., Stiegler P. Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res. 1981 Jan 10;9(1):133–148. doi: 10.1093/nar/9.1.133. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES