Biochemical Genetics

, Volume 47, Issue 9–10, pp 635–644 | Cite as

Long-Term Evolution of 5S Ribosomal DNA Seems to Be Driven by Birth-and-Death Processes and Selection in Ensis Razor Shells (Mollusca: Bivalvia)

  • Joaquín Vierna
  • Ana M. González-Tizón
  • Andrés Martínez-LageEmail author


A study of nucleotide sequence variation of 5S ribosomal DNA from six Ensis species revealed that several 5S ribosomal DNA variants, based on differences in their nontranscribed spacers (NTS), occur in Ensis genomes. The 5S rRNA gene was not very polymorphic, compared with the NTS region. The phylogenetic analyses performed showed a between-species clustering of 5S ribosomal DNA variants. Sequence divergence levels between variants were very large, revealing a lack of sequence homogenization. These results strongly suggest that the long-term evolution of Ensis 5S ribosomal DNA is driven by birth-and-death processes and selection.


5S ribosomal DNA Birth-and-death evolution Ensis Mollusca Bivalvia 



We thank K. Thomas Jensen, Anne S. Lousdal, Ana de la Torriente, Rudo von Cosel, Virginie Héros, and Barbara Buge for providing us with some of the specimens studied. We are in debt to Ángeles Cid for her invaluable help. The support of the Consellería de Educación e Ordenación Universitaria (Xunta de Galicia, Spain) is greatly appreciated.


  1. Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580PubMedCrossRefGoogle Scholar
  2. Brown DD, Sugimoto K (1974) The structure and evolution of ribosomal and 5S DNAs in Xenopus laevis and Xenopus mulleri. Cold Spring Harb Symp Quant Biol 38:501–505PubMedGoogle Scholar
  3. Caradonna F, Bellavia D, Clemente AM, Sisino G, Barbieri R (2007) Chromosomal localization and molecular characterization of three different 5S ribosomal DNA clusters in the sea urchin Paracentrotus lividus. Genome 50:867–870PubMedCrossRefGoogle Scholar
  4. Daniels LM, Delany ME (2003) Molecular and cytogenetic organization of the 5S ribosomal DNA array in chicken (Gallus gallus). Chromosome Res 11:305–317PubMedCrossRefGoogle Scholar
  5. Danna KJ, Workman R, Coryell V, Keim P (1996) 5S rRNA genes in tribe Phaseoleae: array size, number, and dynamics. Genome 39:445–455PubMedCrossRefGoogle Scholar
  6. Eickbush TH, Eickbush DG (2007) Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 175:477–485PubMedCrossRefGoogle Scholar
  7. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  8. Fernández-Tajes J, Méndez J (2007) Identification of the razor clam species Ensis arcuatus, E. siliqua, E. directus, E. macha, and Solen marginatus using PCR-RFLP analysis of the 5S rDNA region. J Agric Food Chem 55:7278–7282PubMedCrossRefGoogle Scholar
  9. Freire R, Insua A, Méndez J (2005) Cerastoderma glaucum 5S ribosomal DNA: characterization of the repeat unit, divergence with respect to Cerastoderma edule, and PCR-RFLPs for the identification of both cockles. Genome 48:427–442PubMedCrossRefGoogle Scholar
  10. Fujiwara M, Inafuku J, Takeda A, Watanabe A, Fujiwara A, Kohno S, Kubota S (2009) Molecular organization of 5S rDNA in bitterlings (Cyprinidae). Genetica 135:355–365PubMedCrossRefGoogle Scholar
  11. Giegerich R, Meyer F, Schleiermacher C (1996) GeneFisher: software support for the detection of postulated genes. Proc Int Conf Intell Syst Mol Biol 4:68–77PubMedGoogle Scholar
  12. Gornung E, Colangelo P, Annesi F (2007) 5S ribosomal RNA genes in six species of Mediterranean grey mullets: genomic organization and phylogenetic inference. Genome 50:787–795PubMedCrossRefGoogle Scholar
  13. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  14. Insua A, Freire R, Ríos J, Méndez J (2001) The 5S rDNA of mussels Mytilus galloprovincialis and M. edulis: sequence variation and chromosomal location. Chromosome Res 9:495–505PubMedCrossRefGoogle Scholar
  15. Keller I, Chintauan-Marquier IC, Veltsos P, Nichols RA (2006) Ribosomal DNA in the grasshopper Podisma pedestris: escape from concerted evolution. Genetics 174:863–874PubMedCrossRefGoogle Scholar
  16. Kumar S, Tamura K, Nei M (2004) Mega3: integrated software for molecular evolutionary genetic analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  17. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948PubMedCrossRefGoogle Scholar
  18. Leo NP, Barker SC (2002) Intragenomic variation in ITS2 rDNA in the louse of humans, Pediculus humanus: ITS2 is not a suitable marker for population studies in this species. Insect Mol Biol 11:651–657PubMedCrossRefGoogle Scholar
  19. Li WH (1989) A statistical test of phylogenies estimated from sequence data. Mol Biol Evol 6:424–435PubMedGoogle Scholar
  20. Li Z, Huang S, Jin W, Ning S, Song Y, Li L (2002) Determination of copy number for 5S rDNA and centromeric sequence RCS2 in rice by Fiber-FISH. Chin Sci Bull 47:214–217CrossRefGoogle Scholar
  21. Little RD, Braaten BC (1989) Genomic organization of human 5S rDNA and sequence of one tandem repeat. Genomics 4:376–383PubMedCrossRefGoogle Scholar
  22. López-Piñón MJ, Freire R, Insua A, Méndez J (2008) Sequence characterization and phylogenetic analysis of the 5S ribosomal DNA in some scallops (Bivalvia: Pectinidae). Hereditas 145:9–19PubMedCrossRefGoogle Scholar
  23. Martins C, Galetti PM (2001) Two 5S rDNA arrays in Neotropical fish species: is it a general rule for fishes? Genetica 111:439–446PubMedCrossRefGoogle Scholar
  24. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  25. Nei M, Hughes AL (1992) Balanced polymorphism and evolution by the birth-and-death process in the MHC loci. In: Tsuji K, Aizawa M, Sasazuki T (eds) 11th Histocompatibility workshop and conference. Oxford University Press, Oxford (UK), pp 27–38Google Scholar
  26. Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121–152PubMedCrossRefGoogle Scholar
  27. Nei M, Stephens JC, Saitou N (1985) Methods for computing the standard errors of branching points in an evolutionary tree and their application to molecular data from humans and apes. Mol Biol Evol 2:66–85PubMedGoogle Scholar
  28. Robles F, de la Herrán R, Ludwig A, Ruiz Rejón C, Ruiz Rejón M, Garrido-Ramos MA (2005) Genomic organization and evolution of the 5S ribosomal DNA in the ancient fish sturgeon. Genome 48:18–28PubMedCrossRefGoogle Scholar
  29. Rooney AP (2004) Mechanisms underlying the evolution and maintenance of functionally heterogeneous 18S rRNA genes in apicomplexans. Mol Biol Evol 21:1704–1711PubMedCrossRefGoogle Scholar
  30. Rooney AP, Ward TJ (2005) Evolution of large ribosomal RNA multigene family in filamentous fungi: birth and death of a concerted evolution paradigm. Proc Natl Acad Sci USA 102:5084–5098PubMedCrossRefGoogle Scholar
  31. Rozas J, Sánchez-Del Barrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  32. Rzhetsky A, Nei M (1992) A simple method for estimating and testing minimum-evolution trees. Mol Biol Evol 9:945–967Google Scholar
  33. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  34. Sword GA, Senior LB, Gaskin JF, Joern A (2007) Double trouble for grasshopper molecular systematics: intra-individual heterogeneity of both mitochondrial 12S-valine-16S and nuclear internal transcribed spacer ribosomal DNA sequences in Hesperotettix viridis (Orthoptera: Acrididae). Syst Entomol 32:420–428CrossRefGoogle Scholar
  35. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  36. Wood V, Gwilliam R, Rajandream MA, Lyne M, Lyne R, Stewart A, Sgouros J, Peat N, Hayles J, Baker S et al (2002) The genome sequence of Schizosaccharomyces pombe. Nature 415:871–880PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Joaquín Vierna
    • 1
  • Ana M. González-Tizón
    • 1
  • Andrés Martínez-Lage
    • 1
    Email author
  1. 1.Department of Molecular and Cell Biology, Evolutionary Biology Group (GIBE)Universidade da CoruñaLa CoruñaSpain

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