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Evolution of a Unique Mitotype-Specific Protein-Coding Extension of the Cytochrome c Oxidase II Gene in Freshwater Mussels (Bivalvia: Unionoida)

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Abstract

A unique mode of mitochondrial DNA inheritance, designated doubly-uniparental inheritance (DUI), occurs in three bivalve subclasses (Pteriomorpha: Mytiloida, Palaeoheterodonta: Unionoida, Heterodonta: Veneroida), indicating that DUI may be a widespread phenomenon among bivalves. In mytiloids, breakdown of this pattern of inheritance (gender-switching) is observed in natural populations and in a phylogenetic context. In contrast, gender-switching has not occurred during the evolutionary history of unionoids. Here we present sequences for the male (M) and female (F) mitotypes from an additional 8 species of Unionoida. Consistent with previous observations, the M and F mitotypes of all species form reciprocally monophyletic clades supporting the hypothesis of taxon-specific rates of gender-switching. Coinciding with the absence of gender-switching is an ≈185 codon extension of the cytochrome c oxidase II (MTCO2) locus in the male genome. The extension is present in all 12 unionoid species examined, including a representative of the family Margaritiferidae, indicating that this protein-coding polymorphism originated ≥ 200 MYBP. Although the extension is well conserved in length among 11 of the 12 species, one taxon has a significantly shortened extension. Lastly, examination of the rates and patterns of substitution indicate that the extension is evolving under relaxed purging selection, a pattern inconsistent with the conserved nature of MTCO2 or any cytochrome c oxidase locus.

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References

  • Beitz E (2000) TEXshade: shading and labeling multiple sequence alignments using LATEX2. Bioinformatics 16:135–139

    Article  PubMed  Google Scholar 

  • Berry DA, Lindgren BW (1996) Statistics: theory and methods, 2nd ed. International Thompson Publishing, London

    Google Scholar 

  • Boore J, Brown W (1994) Complete DNA sequence of the mitochondrial genome of the black chiton, Katharina tunicata. Genetics 138:423–443

    PubMed  Google Scholar 

  • Campbell NJ, Barker SC (1999) The novel mitochondrial gene arrangement of the cattle tick, Boophilus microplusi: fivefold tandem repetition of a coding region. Mol Biol Evol 16:732–740

    PubMed  Google Scholar 

  • Curole JP (2004) Universal primers for the specific amplification of the male mitotype of the Unionoidea (Bivalvia). Cons Gen 5:733–735

    Article  Google Scholar 

  • Curole JP, Kocher TD (2002) Ancient sex-specific extension of the cy-tochrome c oxidase II gene in bivalves and the fidelity of doubly-uniparental inheritance. Mol Biol Evol 19:1323–1328

    PubMed  Google Scholar 

  • Felsenstein J (1985) Phytogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Fisher C, Skibinski D (1990) Sex-biased mitochondrial DNA heteroplasmy in the marine mussel Mytilus. Proc R Soc Lond B Biol Sci 242:149–156

    Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mob Mar Biol Biotechnol 3:294–299

    PubMed  Google Scholar 

  • Frank S, Hurst L (1996) Mitochondria and male disease. Nature 383:224

    Article  PubMed  Google Scholar 

  • Graf DL (2000) The Etherioidea revisited: a phylogenetic analysis of hyriid relationships (Mollusca: Bivalvia: Paleoheterodonta: Unionoida). Occas Pap Mus Zool Univ Mich 729:1–21

    Google Scholar 

  • Graf D, ÓFoighil D (2000) The evolution of brooding characters among the freshwater pearly mussels (Bivalvia: Unionoidea) of North America. J Moll Stud 66:157–170

    Article  Google Scholar 

  • Graur D, Martin W (2004) Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. Trends Genet 20:80–86

    Article  PubMed  Google Scholar 

  • Heard WH, Guckert RH (1970) A re-evaluation of the recent Unionacea (Pelecypoda) of North America. Malacalogia 10:333–335

    Google Scholar 

  • Hoeh W, Blakley K, Brown W (1991) Heteroplasmy suggest limited biparental inheritance of Mytilus mitochondrial DNA. Science 251:1488–1490

    PubMed  Google Scholar 

  • Hoeh W, Stewart D, Sutherland B, Zouros E (1996) Multiple origins of gender-associated mitochondrial DNA lineages in bivalves (Mollusca: Bivalvia). Evolution 50:2276–2286

    Google Scholar 

  • Hoeh WR, Stewart DT, Saavedra C, Sutherland BW, Zouros E (1997) Phylo-genetic evidence for role-reversals of gender-associated mitochondrial DNA in Mytilus (Bivalvia: Mytilidae). Mol Biol Evol 14:959–967

    PubMed  Google Scholar 

  • Hoeh WR, Black MB, Gustafson R, Bogan AE, Lutz RA, Vrijenhoek RC (1998) Testing alternative hypotheses of Neotrigonia (Bivalvia: Trigonioida) phylogenetic relationships using cytochrome c oxidase subunit I sequences. Malacalogia 40:267–278

    Google Scholar 

  • Hoeh WR, Bogan AE, Heard WH (2001) A phylogenetic perspective on the evolution of morphological and reproductive characteristics in the Unionoida. In: Bauer G, Wachtler K (eds) Ecology and evolution of the freshwater mussels Unionoida. Springer, Berlin, pp 257–280

    Google Scholar 

  • Hoeh WR, Stewart DT, Guttman SI (2002) High fidelity of mitochondrial genome transmission under the doubly uniparental mode of inheritance in fresh-water mussels (Bivalvia: Unionoidea). Evolution 56:2252–2261

    PubMed  Google Scholar 

  • Hoffman R, Boore J, Brown W (1992) A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics 131:397–412

    PubMed  Google Scholar 

  • Inoue JG, Miya M, Tsukamoto K, Nishida M (2003) Evolution of the deep-sea gulper eel mitochondrial genomes: large-scale gene rearrangements originated within the eels. Mol Biol Evol 20:1917–1924

    Article  PubMed  Google Scholar 

  • Liu HP, Mitton J, Wu SK (1996) Paternal mitochondrial DNA differentiation far exceeds maternal mitochondrial DNA and allozyme differentiation in the freshwater mussel, Anodonta grandis grandis. Evolution 50:952–957

    Google Scholar 

  • Lydeard C, Mulvey M, Davis G (1996) Molecular systematics and evolution of reproductive traits in North American freshwater unionacean mussels (Mollusca: Bivalvia) as inferred from 16S rRNA gene sequences. Philos Trans R Soc London [Biol] 351:1593–1603

    Google Scholar 

  • Mizi A, Zouros E, Moschonas N, Rodakis GC (2005) The complete maternal and paternal mitochondrial genomes of the Mediterranean mussel Mytilus galloprovincialis: implications for the doubly uniparental inheritance mode of mtDNA. Mol Biol Evol 22:952–967

    Article  PubMed  Google Scholar 

  • Passamonti M, Scali V (2001) Gender-associated mitochondrial DNA hetero-plasmy in the venerid clam Tapes philippinarum (Mollusca: Bivalvia). Currr Genet 39:117–124

    Article  PubMed  Google Scholar 

  • Posada D, Crandall K (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  Google Scholar 

  • Quesada H, Wenne R, Skibinski D (1995) Differential introgression of mitochondrial DNA across species boundaries within the marine mussel genus Mytilus. Proc R Soc Lond B Biol Sci 262:51–56

    Google Scholar 

  • Quesada H, Wenne R, Skibinski DO (1999) Interspecies transfer of female mitochondrial DNA is coupled with role-reversals and departure from neutrality in the mussel Mytilus trossulus. Mol Biol Evol 16:655–665

    PubMed  Google Scholar 

  • Rawson P, Secor C, Hilbish T (1996) The effects of natural hybridization on the regulation of doubly uniparental mtDNA inheritance in blue mussels (Mytilus spp.). Genetics 144:241–248

    PubMed  Google Scholar 

  • Saavedra C, Reyero MI, Zouros E (1997) Male-dependent doubly uniparental inheritance of mitochondrial DNA and female-dependent sex-ratio in the mussel Mytilus galloprovincialis. Genetics 145:1073–1082

    PubMed  Google Scholar 

  • Saccone C, Gissi C, Lanave C, Larizza A, Pesole G, Reyes A (2000) Evolution of the mitochondrial genetic system: an overview. Gene 261:153–159

    Article  PubMed  Google Scholar 

  • Shao R, Barker SC (2003) The highly rearranged mitochondrial genome of the plague thrips, Thrips imaginis (Insecta: Thysanoptera): convergence of two novel gene boundaries and an extraordinary arrangement of rRNA genes. Mol Biol Evol 20:362–370

    Article  PubMed  Google Scholar 

  • Skibinski D, Gallagher C, Beynon C (1994a) Mitochondrial DNA inheritance. Nature 368:817–818

    Article  Google Scholar 

  • Skibinski D, Gallagher C, Beynon C (1994b) Sex-limited mitochondrial DNA transmission in the marine mussel Mytilus edulis. Genetics 138:801–809

    Google Scholar 

  • Smith DG (1976) The distribution of the Margaritiferidae: a review and a new synthesis. Am Mal Bull 24:42(Abstract)

    Google Scholar 

  • Smith DG (2001) Systematics and distribution of the Recent Margaritiferidae. In: Bauer G, Waltcher K (eds) Evolution of the freshwater mussels Unionoida. Springer-Verlag, Berlin, pp 33–50

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTALX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Res 25:4876–4882

    Article  PubMed  Google Scholar 

  • Wenne R, Skibinski D (1996) Mitochondrial DNA heteroplasmy in European populations of the mussel Mytilus trossulus. Marine Biol 122:619–625

    Article  Google Scholar 

  • Wood A, Turner G, Skibinski DO, Beaumont A (2003) Disruption of doubly uniparental inheritance of mitochondrial DNA in hybrid mussels (Mytilus edulis × M. galloprovincialis). Heredity 91:354–360

    Article  PubMed  Google Scholar 

  • Yang Z, Nielsen R, Goldman N, Pederson AMK (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449

    PubMed  Google Scholar 

  • Zeh JA (2004) Sexy sons: a dead end for cytoplasmic genes. Proc R Soc Lond B Biol Sci 271:S306–S309

    Google Scholar 

  • Zouros E (2000) The exceptional mitochondrial DNA system of the mussel family Mytilidae. Genes Genet Syst 75:313–318

    Article  PubMed  Google Scholar 

  • Zouros E, Freeman K, Ball A, Pogson G (1992) Direct evidence for extensive paternal mitochondrial DNA inheritance in the marine mussel Mytilus. Nature 359:412–414

    Article  PubMed  Google Scholar 

  • Zouros E, Ball A, Saavedra C, Freeman K (1994a) Mitochondrial DNA inheritance. Nature 368:818

    Article  Google Scholar 

  • Zouros E, Ball A, Saavedra C, Freeman K (1994b) An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proc Natl Acad Sci USA 91:7463–7467

    Google Scholar 

Download references

Acknowledgments

We thank Dennis Hedgecock and four anonymous reviewers for comments on the manuscript.

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Authors and Affiliations

  1. Hubbard Center for Genome Studies, University of New Hampshire, Durham, New Hampshire, 03824, USA

    Jason P. Curole & Thomas D. Kocher

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  1. Jason P. Curole
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  2. Thomas D. Kocher
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Correspondence to Jason P. Curole.

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[Reviewing Editor: Dr. J. William Ballard]

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Curole, J.P., Kocher, T.D. Evolution of a Unique Mitotype-Specific Protein-Coding Extension of the Cytochrome c Oxidase II Gene in Freshwater Mussels (Bivalvia: Unionoida). J Mol Evol 61, 381–389 (2005). https://doi.org/10.1007/s00239-004-0192-7

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  • DOI: https://doi.org/10.1007/s00239-004-0192-7

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