Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1998 Jul;149(3):1511–1526. doi: 10.1093/genetics/149.3.1511

Nonneutral evolution and differential mutation rate of gender-associated mitochondrial DNA lineages in the marine mussel Mytilus.

H Quesada 1, M Warren 1, D O Skibinski 1
PMCID: PMC1460237  PMID: 9649538

Abstract

Mussels have two types of mitochondrial DNA (mtDNA). The M type is transmitted paternally, and the F type is transmitted maternally. To test hypotheses of the molecular evolution of both mtDNA genomes, 50 nucleotide sequences were obtained for 396 bp of the COIII gene of European populations of Mytilus edulis and the Atlantic and Mediterranean forms of M. galloprovincialis. Analysis based on the proportion of synonymous and nonsynonymous substitutions indicate that mtDNA is evolving in a non-neutral and complex fashion. Previous studies on American mussels demonstrated that the F genome experiences a higher purifying selection and that the M genome evolves faster. Here we show that these patterns also hold in European populations. However, in contrast to American populations, where an excess of replacement substitution between F and M lineages has been reported, a significant excess of replacement polymorphism within mtDNA lineages is observed in European populations of M. galloprovincialis. European populations also show an excess of replacement polymorphism within the F but not within the M genome with respect to American M. trossulus, as well as a consistent pattern of excess of rare variants in both F and M genomes. These results are consistent with a nearly neutral model of molecular evolution and a recent relaxation of selective constraints on European mtDNA. Levels of diversity are significantly higher for the M than F genome, and the M genome also accumulates synonymous and nonsynonymous substitutions at a higher rate, in contrast with earlier reports where no difference for the synonymous rate was observed. It is suggested that a subtle balance between relaxed selection and a higher mutation rate explains the faster evolutionary rate of the M lineage.

Full Text

The Full Text of this article is available as a PDF (320.7 KB).

Selected References

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

  1. Ballard J. W., Kreitman M. Unraveling selection in the mitochondrial genome of Drosophila. Genetics. 1994 Nov;138(3):757–772. doi: 10.1093/genetics/138.3.757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Birky C. W., Jr, Walsh J. B. Effects of linkage on rates of molecular evolution. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6414–6418. doi: 10.1073/pnas.85.17.6414. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brookfield J. F., Sharp P. M. Neutralism and selectionism face up to DNA data. Trends Genet. 1994 Apr;10(4):109–111. doi: 10.1016/0168-9525(94)90201-1. [DOI] [PubMed] [Google Scholar]
  4. Comeron J. M. A method for estimating the numbers of synonymous and nonsynonymous substitutions per site. J Mol Evol. 1995 Dec;41(6):1152–1159. doi: 10.1007/BF00173196. [DOI] [PubMed] [Google Scholar]
  5. Fu Y. X. A phylogenetic estimator of effective population size or mutation rate. Genetics. 1994 Feb;136(2):685–692. doi: 10.1093/genetics/136.2.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Higgins D. G., Thompson J. D., Gibson T. J. Using CLUSTAL for multiple sequence alignments. Methods Enzymol. 1996;266:383–402. doi: 10.1016/s0076-6879(96)66024-8. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Hoeh W. R., Stewart D. T., Sutherland B. W., Zouros E. Cytochrome c oxidase sequence comparisons suggest an unusually high rate of mitochondrial DNA evolution in Mytilus (Mollusca: Bivalvia) Mol Biol Evol. 1996 Feb;13(2):418–421. doi: 10.1093/oxfordjournals.molbev.a025600. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Kaneko M., Satta Y., Matsuura E. T., Chigusa S. I. Evolution of the mitochondrial ATPase 6 gene in Drosophila: unusually high level of polymorphism in D. melanogaster. Genet Res. 1993 Jun;61(3):195–204. doi: 10.1017/s0016672300031360. [DOI] [PubMed] [Google Scholar]
  11. Kaplan N. L., Hudson R. R., Langley C. H. The "hitchhiking effect" revisited. Genetics. 1989 Dec;123(4):887–899. doi: 10.1093/genetics/123.4.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. Nachman M. W., Brown W. M., Stoneking M., Aquadro C. F. Nonneutral mitochondrial DNA variation in humans and chimpanzees. Genetics. 1996 Mar;142(3):953–963. doi: 10.1093/genetics/142.3.953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Quesada H., Beynon C. M., Skibinski D. O. A mitochondrial DNA discontinuity in the mussel Mytilus galloprovincialis Lmk: pleistocene vicariance biogeography and secondary intergradation. Mol Biol Evol. 1995 May;12(3):521–524. doi: 10.1093/oxfordjournals.molbev.a040227. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Rand D. M., Kann L. M. Excess amino acid polymorphism in mitochondrial DNA: contrasts among genes from Drosophila, mice, and humans. Mol Biol Evol. 1996 Jul;13(6):735–748. doi: 10.1093/oxfordjournals.molbev.a025634. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Rawson P. D., Secor C. L., Hilbish T. J. The effects of natural hybridization on the regulation of doubly uniparental mtDNA inheritance in blue mussels (Mytilus spp.). Genetics. 1996 Sep;144(1):241–248. doi: 10.1093/genetics/144.1.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rozas J., Rozas R. DnaSP version 2.0: a novel software package for extensive molecular population genetics analysis. Comput Appl Biosci. 1997 Jun;13(3):307–311. [PubMed] [Google Scholar]
  21. Saavedra C., Stewart D. T., Stanwood R. R., Zouros E. Species-specific segregation of gender-associated mitochondrial DNA types in an area where two mussel species (Mytilus edulis and M. trossulus) hybridize. Genetics. 1996 Jul;143(3):1359–1367. doi: 10.1093/genetics/143.3.1359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Stewart D. T., Kenchington E. R., Singh R. K., Zouros E. Degree of selective constraint as an explanation of the different rates of evolution of gender-specific mitochondrial DNA lineages in the mussel mytilus. Genetics. 1996 Jul;143(3):1349–1357. doi: 10.1093/genetics/143.3.1349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. 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]
  25. Zouros E., Oberhauser Ball A., Saavedra C., Freeman K. R. An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7463–7467. doi: 10.1073/pnas.91.16.7463. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES