Skip to main content
Genetics logoLink to Genetics
. 2003 Jun;164(2):603–611. doi: 10.1093/genetics/164.2.603

Molecular evolution and recombination in gender-associated mitochondrial DNAs of the Manila clam Tapes philippinarum.

Marco Passamonti 1, Jeffrey L Boore 1, Valerio Scali 1
PMCID: PMC1462575  PMID: 12807780

Abstract

Doubly uniparental inheritance (DUI) provides an intriguing system for addressing aspects of molecular evolution and intermolecular recombination of mitochondrial DNA. For this reason, a large sequence analysis has been performed on Tapes philippinarum (Bivalvia, Veneridae), which has mitochondrial DNA heteroplasmy that is consistent with a DUI. The sequences of a 9.2-kb region (containing 29 genes) from 9 individuals and the sequences of a single gene from another 44 individuals are analyzed. Comparisons suggest that the two sex-related mitochondrial genomes do not experience a neutral pattern of divergence and that selection may act with varying strength on different genes. This pattern of evolution may be related to the long, separate history of M and F genomes within their tissue-specific "arenas." Moreover, our data suggest that recombinants, although occurring in soma, may seldom be transmitted to progeny in T. philippinarum.

Full Text

The Full Text of this article is available as a PDF (192.7 KB).

Selected References

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

  1. Arctander P. Mitochondrial recombination? Science. 1999 Jun 25;284(5423):2090–2091. doi: 10.1126/science.284.5423.2089e. [DOI] [PubMed] [Google Scholar]
  2. Awadalla P., Eyre-Walker A., Smith J. M. Linkage disequilibrium and recombination in hominid mitochondrial DNA. Science. 1999 Dec 24;286(5449):2524–2525. doi: 10.1126/science.286.5449.2524. [DOI] [PubMed] [Google Scholar]
  3. Betrán E., Rozas J., Navarro A., Barbadilla A. The estimation of the number and the length distribution of gene conversion tracts from population DNA sequence data. Genetics. 1997 May;146(1):89–99. doi: 10.1093/genetics/146.1.89. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Boore J. L. Animal mitochondrial genomes. Nucleic Acids Res. 1999 Apr 15;27(8):1767–1780. doi: 10.1093/nar/27.8.1767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Boore J. L., Brown W. M. Complete sequence of the mitochondrial DNA of the annelid worm Lumbricus terrestris. Genetics. 1995 Sep;141(1):305–319. doi: 10.1093/genetics/141.1.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dalziel Anne C., Stewart Donald T. Tissue-specific expression of male-transmitted mitochondrial DNA and its implications for rates of molecular evolution in Mytilus mussels (Bivalvia: Mytilidae). Genome. 2002 Apr;45(2):348–355. doi: 10.1139/g01-159. [DOI] [PubMed] [Google Scholar]
  8. Dean F. B., Nelson J. R., Giesler T. L., Lasken R. S. Rapid amplification of plasmid and phage DNA using Phi 29 DNA polymerase and multiply-primed rolling circle amplification. Genome Res. 2001 Jun;11(6):1095–1099. doi: 10.1101/gr.180501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Elson J. L., Andrews R. M., Chinnery P. F., Lightowlers R. N., Turnbull D. M., Howell N. Analysis of European mtDNAs for recombination. Am J Hum Genet. 2000 Dec 11;68(1):145–153. doi: 10.1086/316938. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Eyre-Walker A., Awadalla P. Does human mtDNA recombine? J Mol Evol. 2001 Oct-Nov;53(4-5):430–435. doi: 10.1007/s002390010232. [DOI] [PubMed] [Google Scholar]
  11. Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994 Oct;3(5):294–299. [PubMed] [Google Scholar]
  12. Hagelberg E., Goldman N., Lió P., Whelan S., Schiefenhövel W., Clegg J. B., Bowden D. K. Evidence for mitochondrial DNA recombination in a human population of island Melanesia. Proc Biol Sci. 1999 Mar 7;266(1418):485–492. doi: 10.1098/rspb.1999.0663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hoeh W. R., Stewart D. T., Saavedra C., Sutherland B. W., Zouros E. Phylogenetic evidence for role-reversals of gender-associated mitochondrial DNA in Mytilus (Bivalvia: Mytilidae). Mol Biol Evol. 1997 Sep;14(9):959–967. doi: 10.1093/oxfordjournals.molbev.a025839. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. 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]
  16. Ingman M., Kaessmann H., Päbo S., Gyllensten U. Mitochondrial genome variation and the origin of modern humans. Nature. 2000 Dec 7;408(6813):708–713. doi: 10.1038/35047064. [DOI] [PubMed] [Google Scholar]
  17. Kajander O. A., Rovio A. T., Majamaa K., Poulton J., Spelbrink J. N., Holt I. J., Karhunen P. J., Jacobs H. T. Human mtDNA sublimons resemble rearranged mitochondrial genoms found in pathological states. Hum Mol Genet. 2000 Nov 22;9(19):2821–2835. doi: 10.1093/hmg/9.19.2821. [DOI] [PubMed] [Google Scholar]
  18. Kivisild T., Villems R. Questioning evidence for recombination in human mitochondrial DNA. Science. 2000 Jun 16;288(5473):1931–1931. [PubMed] [Google Scholar]
  19. Lowe T. M., Eddy S. R. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997 Mar 1;25(5):955–964. doi: 10.1093/nar/25.5.955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Preiss A., Hartley D. A., Artavanis-Tsakonas S. The molecular genetics of Enhancer of split, a gene required for embryonic neural development in Drosophila. EMBO J. 1988 Dec 1;7(12):3917–3927. doi: 10.1002/j.1460-2075.1988.tb03278.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Päbo S., Irwin D. M., Wilson A. C. DNA damage promotes jumping between templates during enzymatic amplification. J Biol Chem. 1990 Mar 15;265(8):4718–4721. [PubMed] [Google Scholar]
  23. Quesada H., Warren M., Skibinski D. O. Nonneutral evolution and differential mutation rate of gender-associated mitochondrial DNA lineages in the marine mussel Mytilus. Genetics. 1998 Jul;149(3):1511–1526. doi: 10.1093/genetics/149.3.1511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. 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]
  27. Thyagarajan B., Padua R. A., Campbell C. Mammalian mitochondria possess homologous DNA recombination activity. J Biol Chem. 1996 Nov 1;271(44):27536–27543. doi: 10.1074/jbc.271.44.27536. [DOI] [PubMed] [Google Scholar]
  28. Wolstenholme D. R. Animal mitochondrial DNA: structure and evolution. Int Rev Cytol. 1992;141:173–216. doi: 10.1016/s0074-7696(08)62066-5. [DOI] [PubMed] [Google Scholar]
  29. Zhang J., Kumar S., Nei M. Small-sample tests of episodic adaptive evolution: a case study of primate lysozymes. Mol Biol Evol. 1997 Dec;14(12):1335–1338. doi: 10.1093/oxfordjournals.molbev.a025743. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. 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