Advertisement

A Rigorous Analysis of the Pattern of Intron Conservation Supports the Coelomata Clade of Animals

  • Jie Zheng
  • Igor B. Rogozin
  • Eugene V. Koonin
  • Teresa M. Przytycka
Part of the Lecture Notes in Computer Science book series (LNCS, volume 4751)

Abstract

Many intron positions are conserved in varying subsets of eukaryotic genomes and, consequently, comprise a potentially informative class of phylogenetic characters. Roy and Gilbert developed a method of phylogenetic reconstruction using the patterns of intron presence-absence in eukaryotic genes and, applying this method to the analysis of animal phylogeny, obtained support for an Ecdysozoa clade ([1]). The critical assumption in the method was the independence of the rates of intron loss in different branches of the phylogenetic. Here, this assumption is refuted by showing that the branch-specific intron loss rates are strongly correlated. We show that different tree topologies are obtained, in each case with a significant statistical support, when different subsets of intron positions are analyzed. The analysis of the conserved intron positions supports the Coelomata topology, i.e., a clade comprised of arthropods and chordates, whereas the analysis of more variable intron positions favors the Ecdysozoa topology, i.e., a clade of arthropods and nematodes. We show, however, that the support for Ecdysozoa is fully explained by parallel loss of introns in nematodes and arthropods, a factor that does not contribute to the analysis of the conserved introns. The developed procedure for the identification and analysis of conserved introns and other characters with minimal or no homoplasy is expected to be useful for resolving many hard phylogenetic problems.

Keywords

Retention Rate Tree Topology Intron Position Variable Intron Intron Loss 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Roy, S.W., Gilbert, W.: Resolution of a deep animal divergence by the pattern of intron conservation. Proc. Natl. Acad. Sci. U S A 102, 4403–4408 (2005)CrossRefGoogle Scholar
  2. 2.
    Felsenstein, J.: Inferring Phylogenies. Sinauer Associates, Sunderland, MA (2004)Google Scholar
  3. 3.
    Snel, B., Bork, P., Huynen, M.A.: Genome phylogeny based on gene content. Nat. Genet. 21, 108–110 (1999)CrossRefGoogle Scholar
  4. 4.
    Wolf, Y.I., Rogozin, I.B., Grishin, N.V., Tatusov, R.L., Koonin, E.V.: Genome trees constructed using five different approaches suggest new major bacterial clades. BMC Evolutionary Biology. 1 (2001)Google Scholar
  5. 5.
    Wolf, Y.I., Rogozin, I.B., Grishin, N.V., Koonin, E.V.: Genome trees and the tree of life. Trends Genet. 18, 472–479 (2002)CrossRefGoogle Scholar
  6. 6.
    Snel, B., Huynen, M.A., Dutilh, B.E.: Genome trees and the nature of genome evolution. Annu. Rev. Microbiol. 59, 191–209 (2005)CrossRefGoogle Scholar
  7. 7.
    Rokas, A., Holland, P.W.: Rare genomic changes as a tool for phylogenetics. Trends in Ecology and Evolution 15, 454–459 (2000)CrossRefGoogle Scholar
  8. 8.
    Nei, M., Kumar, S.: Molecular Evolution and Phylogenetics. Oxford Univ, Oxford (2001)Google Scholar
  9. 9.
    Delsuc, F., Brinkmann, H., Philippe, H.: Phylogenomics and the reconstruction of the tree of life. Nat. Rev. Genet. 6, 361–375 (2005)CrossRefGoogle Scholar
  10. 10.
    Boore, J.L.: The use of genome-level characters for phylogenetic reconstruction. Trends Ecol. Evol. 21, 439–446 (2006)CrossRefGoogle Scholar
  11. 11.
    Fedorov, A., Merican, A.F., Gilbert, W.: Large-scale comparison of intron positions among animal, plant, and fungal genes. Proc. Natl. Acad. Sci. U S A 99, 16128–16133 (2002)CrossRefGoogle Scholar
  12. 12.
    Rogozin, I.B., Wolf, Y.I., Sorokin, A.V., Mirkin, B.G., Koonin, E.V.: Remarkable interkingdom conservation of intron positions and massive, lineage-specific intron loss and gain in eukaryotic evolution. Curr. Biol. 13, 1512–1517 (2003)CrossRefGoogle Scholar
  13. 13.
    Sverdlov, A.V., Rogozin, I.B., Babenko, V.N., Koonin, E.V.: Conservation versus parallel gains in intron evolution. Nucleic Acids Res. 33, 1741–1748 (2005)CrossRefGoogle Scholar
  14. 14.
    Brusca, R.C., Brusca, G.J.: Invertebrates. Sinauer Associates, Sunderland, Mass (1990)Google Scholar
  15. 15.
    Raff, R.A: The Shape of Life: Genes, Development, and the Evolution of Animal Form. University of Chicago Press, Chicago, IL (1996)Google Scholar
  16. 16.
    Haeckel, E.: Generelle Morphologie der Organismen. G.Reimer, Berlin (1866)Google Scholar
  17. 17.
    Field, K.G., Olsen, G.J., Lane, D.J., Giovannoni, S.J., Ghiselin, M.T., Raff, E.C., Pace, N.R., Raff, R.A.: Molecular phylogeny of the animal kingdom. Science 239, 748–753 (1988)CrossRefGoogle Scholar
  18. 18.
    Turbeville, J.M., Pfeifer, D.M., Field, K.G., Raff, R.A.: The phylogenetic status of arthropods, as inferred from 18s rrna sequences. Mol. Biol. Evol. 8, 669–686 (1991)Google Scholar
  19. 19.
    Aguinaldo, A.M., Turbeville, J.M., Linford, L.S., Rivera, M.C., Garey, J.R., Raff, R.A., Lake, J.A.: Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387, 489–493 (1997)CrossRefGoogle Scholar
  20. 20.
    Telford, M.J., Copley, R.R.: Animal phylogeny: fatal attraction. Curr. Biol. 15, 296–299 (2005)CrossRefGoogle Scholar
  21. 21.
    Felsenstein, J.: Cases in which parsimony or compatibility methods will be positively misleading. Syst. Zool. 27, 401–410 (1978)CrossRefGoogle Scholar
  22. 22.
    Reyes, A., Pesole, G., Saccone, C.: Long-branch attraction pheonomenon and the impact of among-site rate variation on rodent phylogeny. Gene 259, 177–187 (2000)CrossRefGoogle Scholar
  23. 23.
    Philippe, H., Lartillot, N., Brinkmann, H.: Multigene analyses of bilaterian animals corroborate the monophyly of ecdysozoa, lophotrochozoa, and protostomia. Mol. Biol. Evol. 22, 1246–1253 (2005)CrossRefGoogle Scholar
  24. 24.
    Giribet, G., Distel, D.L., Polz, M., Sterrer, W., Wheeler, W.C.: Triploblastic relationships with emphasis on the acoelomates and the position of gnathostomulida, cycliophora, plathelminthes, and chaetognatha: a combined approach of 18s rdna sequences and morphology. Syst. Biol. 49, 539–562 (2000)CrossRefGoogle Scholar
  25. 25.
    Peterson, K.J., Eernisse, D.J.: Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18s rdna gene sequences. Evol. Dev. 3, 170–205 (2001)CrossRefGoogle Scholar
  26. 26.
    Mallatt, J., Winchell, C.J.: Testing the new animal phylogeny: first use of combined large-subunit and small-subunit rrna gene sequences to classify the protostomes. Mol. Biol. Evol. 19, 289–301 (2002)Google Scholar
  27. 27.
    de Rosa, R., Grenier, J.K., Andreeva, T., Cook, C.E., Adoutte, A., Akam, M., Carroll, S.B., Balavoine, G.: Hox genes in brachiopods and priapulids and protostome evolution. Nature 399, 772–776 (1999)CrossRefGoogle Scholar
  28. 28.
    Manuel, M., Kruse, M., Muller, W.E., Parco, Y.L.: The comparison of beta-thymosin homologues among metazoa supports an arthropod-nematode clade. J. Mol. Evol. 51, 378–381 (2000)Google Scholar
  29. 29.
    Adoutte, A., Balavoine, G., Lartillot, N., Lespinet, O., Prud’homme, B., de Rosa, R.: The new animal phylogeny: reliability and implications. Proc. Natl. Acad. Sci. U S A 97, 4453–4456 (2000)CrossRefGoogle Scholar
  30. 30.
    Valentine, J.W., Collins, A.G.: The significance of moulting in ecdysozoan evolution. Evol. Dev. 2, 152–156 (2000)CrossRefGoogle Scholar
  31. 31.
    Collins, A.G., Valentine, J.W.: Defining phyla: evolutionary pathways to metazoan body plans. Evol. Dev. 3, 432–442 (2001)CrossRefGoogle Scholar
  32. 32.
    Telford, M.J., Budd, G.E.: The place of phylogeny and cladistics in evo-devo research. Int. J. Dev. Biol. 47, 479–490 (2003)Google Scholar
  33. 33.
    Mushegian, A.R., Garey, J.R., Martin, J., Liu, L.X.: Large-scale taxonomic profiling of eukaryotic model organisms: a comparison of orthologous proteins encoded by the human, fly, nematode, and yeast genomes. Genome Res. 8, 590–598 (1998)Google Scholar
  34. 34.
    Blair, J.E., Ikeo, K., Gojobori, T., Hedges, S.B.: The evolutionary position of nematodes. BMC Evol. Biol. 2(7) (2002)Google Scholar
  35. 35.
    Wolf, Y.I., Rogozin, I.B., Koonin, E.V.: Coelomata and not ecdysozoa: evidence from genome-wide phylogenetic analysis. Genome Res. 14, 29–36 (2004)CrossRefGoogle Scholar
  36. 36.
    Stuart, G.W., Berry, M.W.: An svd-based comparison of nine whole eukaryotic genomes supports a coelomate rather than ecdysozoan lineage. BMC Bioinformatics 5, 204 (2004)CrossRefGoogle Scholar
  37. 37.
    Philip, G.K., Creevey, C.J., McInerney, J.O.: The opisthokonta and the ecdysozoa may not be clades: stronger support for the grouping of plant and animal than for animal and fungi and stronger support for the coelomata than ecdysozoa. Mol. Biol. Evol. 22, 1175–1184 (2005)CrossRefGoogle Scholar
  38. 38.
    Zdobnov, E.M., von Mering, C., Letunic, I., Bork, P.: Consistency of genome-based methods in measuring metazoan evolution. FEBS Lett. 579, 3355–3361 (2005)CrossRefGoogle Scholar
  39. 39.
    Ciccarelli, F.D., Doerks, T., von Mering, C., Creevey, C.J., Snel, B., Bork, P.: Toward automatic reconstruction of a highly resolved tree of life. Science 311, 1283–1287 (2006)CrossRefGoogle Scholar
  40. 40.
    Telford, M.J.: The multimeric beta-thymosin found in nematodes and arthropods is not a synapomorphy of the ecdysozoa. Evol. Dev. 6, 90–94 (2004)CrossRefGoogle Scholar
  41. 41.
    Brinkmann, H., van der Giezen, M., Zhou, Y., de Raucourt, G.P., Philippe, H.: An empirical assessment of long-branch attraction artefacts in deep eukaryotic phylogenomics. Syst. Biol. 54, 743–757 (2005)CrossRefGoogle Scholar
  42. 42.
    Dopazo, H., Dopazo, J.: Genome-scale evidence of the nematode-arthropod clade. Genome Biol 6(5), R41 (2005)CrossRefGoogle Scholar
  43. 43.
    Copley, R.R., Aloy, P., Russell, R.B., Telford, M.J.: Systematic searches for molecular synapomorphies in model metazoan genomes give some support for ecdysozoa after accounting for the idiosyncrasies of caenorhabditis elegans. Evol. Dev. 6, 164–169 (2004)CrossRefGoogle Scholar
  44. 44.
    Lartillot, N., Brinkmann, H., Philippe, H.: Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model. BMC Evol. Biol. Suppl. 1 7, S4 (2007)CrossRefGoogle Scholar
  45. 45.
    Hedges, S.B.: The origin and evolution of model organisms. Nat. Rev. Genet. 3, 838–849 (2002)CrossRefGoogle Scholar
  46. 46.
    Telford, M.J.: Animal phylogeny: back to the coelomata? Curr. Biol. 14, R274–276 (2004)CrossRefGoogle Scholar
  47. 47.
    Jones, M., Blaxter, M.: Evolutionary biology: animal roots and shoots. Nature 434, 1076–1077 (2005)CrossRefGoogle Scholar
  48. 48.
    Rogozin, I.B., Wolf, Y.I., Carmel, L., Koonin, E.V.: Ecdysozoan clade rejected by genome-wide analysis of rare amino acid replacements. Mol. Biol. Evol. 24, 1080–1090 (2007)CrossRefGoogle Scholar
  49. 49.
    Przytycka, T.M.: An important connection between network motifs and parsimony models. In: Apostolico, A., Guerra, C., Istrail, S., Pevzner, P., Waterman, M. (eds.) RECOMB 2006. LNCS (LNBI), vol. 3909, pp. 321–335. Springer, Heidelberg (2006)CrossRefGoogle Scholar
  50. 50.
    Nguyen, H.D, Yoshihama, M., Kenmochi, N.: New maximum likelihood estimators for eukaryotic intron evolution. PLoS Comput. Biol. 1(7), 79 (2005)CrossRefGoogle Scholar
  51. 51.
    Farris, J.S.: Phylogenetic analysis under dollo’s law. Syst. Zool. 26, 77–88 (1977)CrossRefGoogle Scholar
  52. 52.
    Rogozin, I.B., Babenko, V.N., Wolf, Y.I., Koonin, E.V.: Dollo parsimony and reconstruction of genome evolution. In: Albert, V.A. (ed.) Parsimony, Phylogeny, and Genomics, pp. 190–200. Oxford University Press, Oxford (2005)Google Scholar
  53. 53.
    Felsenstein, J.: Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods. Methods Enzymol 266, 418–427 (1996)CrossRefGoogle Scholar
  54. 54.
    Prager, E.M., Wilson, A.C.: Ancient origin of lactalbumin from lysozyme: analysis of dna and amino acid sequences. J. Mol. Evol. 27, 326–335 (1988)CrossRefGoogle Scholar
  55. 55.
    Fedorov, A., Roy, S., Fedorova, L., Gilbert, W.: Mystery of intron gain. Genome Res. 13, 2236–2241 (2003)CrossRefGoogle Scholar
  56. 56.
    Roy, S.W., Penny, D.: Smoke without fire: most reported cases of intron gain in nematodes instead reflect intron losses. Mol. Biol. Evol. 23, 2259–2262 (2006)CrossRefGoogle Scholar
  57. 57.
    Carmel, L., Wolf, Y.I., Rogozin, I.B., Koonin, E.V.: Three distinct modes of intron dynamics in the evolution of eukaryotes. Genome Res. (in press, 2007)Google Scholar
  58. 58.
    Brinkmann, H., Philippe, H.: Archaea sister group of bacteria? indications from tree reconstruction artifacts in ancient phylogenies. Mol. Biol. Evol. 16, 817–825 (1999)Google Scholar
  59. 59.
    Philippe, H., Germot, A., Moreira, D.: The new phylogeny of eukaryotes. Curr. Opin. Genet. Dev. 10, 596–601 (2000)CrossRefGoogle Scholar
  60. 60.
    Brochier, C., Philippe, H.: Phylogeny: a non-hyperthermophilic ancestor for bacteria. Nature 417, 244 (2002)CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2007

Authors and Affiliations

  • Jie Zheng
    • 1
  • Igor B. Rogozin
    • 1
  • Eugene V. Koonin
    • 1
  • Teresa M. Przytycka
    • 1
  1. 1.National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894USA

Personalised recommendations