Are all fishes ancient polyploids?

  • Yves Van de Peer
  • John S. Taylor
  • Axel Meyer


Euteleost fishes seem to have more copies of many genes than their tetrapod relatives. Three different mechanisms could explain the origin of these 'extra' fish genes. The duplicates may have been produced during a fish-specific genome duplication event. A second explanation is an increased rate of independent gene duplications in fish. A third possibility is that after gene or genome duplication events in the common ancestor of fish and tetrapods, the latter lost more genes. These three hypotheses have been tested by phylogenetic tree reconstruction. Phylogenetic analyses of sequences from human, mouse, chicken, frog (Xenopus laevis), zebrafish (Danio rerio) and pufferfish (Takifugu rubripes) suggest that ray-finned fishes are likely to have undergone a whole genome duplication event between 200 and 450 million years ago. We also comment here on the evolutionary consequences of this ancient genome duplication.

genome duplicaiton gene evolution subfunctionalization 


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  1. Altschmied, J., Delfgaauw, J., Wilde, B., Duschl, J., Bouneau, L., Volff, J.-N. and Schartl, M. (2002) Subfunctionalization of duplicate mitf genes associated with differential degeneration of alternative exons in fish. Genetics 161, 259-267.Google Scholar
  2. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402.Google Scholar
  3. Amores, A., Force, A., Yan, Y.-L., Joly, L., Amemiya, C., Fritz, A., Ho, R.K., Langeland, J., Prince, V., Wang, Y.-L., Westerfield, M., Ekker, M. and Postlethwait, J.H. (1998) Zebrafish hox clusters and vertebrate genome evolution. Science, 282,1711-1714.Google Scholar
  4. Aparicio, S., Hawker, K., Cottage, A., Mikawa, Y., Zuo, L., Venkatesh, B., Chen, E., Krumlauf, R. and Brenner, S. (1997) Organization of the Fugu rubripes Hox clusters: evidence for continuing evolution of vertebrate Hox complexes. Nature Genet., 16, 79-83.Google Scholar
  5. Carroll, R.L. (1997) Patterns and Processes of Vertebrate Evolution, Cambridge University Press, Cambridge, UK.Google Scholar
  6. Chiang, E.F., Yan, Y.L., Tong, S.K., Hsiao, P.H., Guiguen, Y., Postlethwaith, J. and Chung, B.C. (2001) Characterization of duplicated zebrafish cyp19 genes. J. Exp. Zool., 290, 709-714.Google Scholar
  7. Davis, C.A., Homyard, D.P., Millen, K.J. and Joyner, A.L. (1991) Examining pattern formation in mouse, chicken and frog embryos with an En-specific antiserum. Development, 2, 287-298.Google Scholar
  8. Ekker, M., Akimenko, M.A., Allende, M.L., Smith, R., Drouin, G., Langille, R.M., Weinberg, E.S. and Westerfield, M. (1997) Relationships among msx gene structure and function in zebrafish and other vertebrates. Mol. Biol. Evol., 14, 1008-1022.Google Scholar
  9. Force, A., Lynch, M., Pickett, F.B., Amores, A., Yan, Y.-l. and Postlethwait, J. (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics, 151, 1531-1545.Google Scholar
  10. Gardner, C.A. and Barald, K.F. (1992) Expression patterns of engrailed-like proteins in the chick embryo. Dev. Dyn., 193, 370-388.Google Scholar
  11. Gates, M.A., Kim, L., Cardozo, T., Sirotkin, H.I., Dougan, S.T., Lashkari, D., Abagyan, R., Schier, A.F. and Talbot, W.S. (1999) A genetic linkage map for zebrafish: comparative analysis and localization of genes and expressed sequences. Genome Res., 9, 334-347.Google Scholar
  12. Gehring, W.J. (1998). Master Control Genes in Development and Evolution: the Homeobox Story. Yale University Press, New HavenGoogle Scholar
  13. Gibson, T.J. and Spring, J. (1998) Genetic redundancy in vertebrates: polyploidy and persistence of genes encoding multidomain proteins. Trends Genet., 14, 46-49.Google Scholar
  14. Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser., 41, 95-98.Google Scholar
  15. Holland, P.W. (1997) Vertebrate evolution: something fishy about Hox genes. Curr. Biol., 7, R570-R572.Google Scholar
  16. Holland, P.W.H. (1999) The effect of gene duplication on homology. In Homology (Eds., Bock, G.R. and Cardew, G.), Wiley, Chichester, UK, pp. 226-242.Google Scholar
  17. Holland, P.W. and Garcia-Fernandez, J. (1996) Hox genes and chordate evolution. Dev. Biol., 173, 382-395.Google Scholar
  18. Hughes, A.L. (1994) The evolution of functionally novel proteins after gene duplication. Proc. R. Soc. Lond. B, 256, 119-124.Google Scholar
  19. Hughes, A.L. (1999) Phylogenies of developmentally important proteins do not support the hypothesis of two rounds of genome duplication early in vertebrate history. J. Mol. Evol., 48, 565-576.Google Scholar
  20. Hughes, A.L., da Silva, J. and Friedman, R. (2001) Ancient genome duplications did not structure the human Hox-bearing chromosomes. Genome Res., 11, 771-780.Google Scholar
  21. Imboden, M., Devignot, V. and Goblet, C. (2001) Phylogenetic relationships and chromosomal location of five distinct glycine receptor subunit genes in the teleost Danio rerio. Dev. Genes Evol., 211, 415-422.Google Scholar
  22. Joyner, A.L. and Martin, G.R. (1987) En-1 and En-2, two mouse genes with sequence homolog to the Drosophila engrailed gene: expression during embryogenesis. Genes Dev., 1, 29-38.Google Scholar
  23. Laforest, L., Brown, C.W., Poleo, G., Geraudie, J., Tada, M., Ekker, M. and Akimenko, M.-A. (1998) Involvement of the Sonic Hedgehog, patched 1 and bmp2 genes in patterning of the zebrafish dermal fin rays. Development, 125, 4175-4184.Google Scholar
  24. Lundin, L.-G. (1999) Gene duplications in early metazoan evolution. Cell Dev. Biol., 10, 523-530.Google Scholar
  25. Lydeard, C. and Roe, K.J. (1997) The phylogenetic utility of the mitochondrial cytochrome b gene for inferring relationships among actinopterygian fishes. In Molecular Systematics of Fishes (Eds., Kocher, T.C. and Stepien, C.A.), Academic Press, San Diego, CA, pp. 285-303.Google Scholar
  26. Lynch, M. and Conery, J.S. (2000) The evolutionary fate and consequences of duplicate genes. Science, 290, 1151-1155.Google Scholar
  27. Lynch, M. and Force, A. (2000a) The probability of duplicate gene preservation by subfunctionalization. Genetics, 154, 459-473.Google Scholar
  28. Lynch, M. and Force, A. (2000b) The origin of interspecific genomic incompatibility via gene duplication. Am. Nat. 156, 590-605.Google Scholar
  29. Málaga-Trillo, E. and Meyer, A. (2001) Genome duplications and accelerated evolution of Hox genes and cluster architecture in teleost fishes. Amer. Zool., 41: 676-686.Google Scholar
  30. Martinez-Barbera, J.P., Toresson, H., Da Rocha, S. and Krauss, S. (1997) Cloning and expression of three members of the zebrafish Bmp family: Bmp2a, Bmp2b and Bmp4. Gene, 198, 53-59.Google Scholar
  31. Mellgren E.M. and Johnson, S.L. (2002) The evolution of morphological complexity in zebrafish stripes. Trends Genet., 18, 128-134.Google Scholar
  32. Meyer, A. and Schartl, M. (1999) Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Curr. Opin. Cell Biol., 11, 699-704.Google Scholar
  33. Naruse, K., Fukamachi, S., Mitani, H., Kondo, M., Matsuoka, T., Kondo, S., Hanamura, N., Morita, Y., Hasegawa, K., Nishigaki, R., Shimada, A., Wada, H., Kusakabe, T., Suzuki, N., Kinoshita, M., Kanamori, A., Terado, T., Kimura, H., Nonaka, M. and Shima, A. (2000) A detailed linkage map of medaka, Oryzias latipes: comparative genomics and genome evolution. Genetics, 154, 1773-1784.Google Scholar
  34. Nelson, J.S. (1994) Fishes of the World, 3rd ed., Wiley, New York, NY.Google Scholar
  35. Nowak, M.A., Boerlijst, M.C., Cooke, J. and Maynard Smith, J. (1997) Evolution of genetic redundancy. Nature, 388, 167-171.Google Scholar
  36. Ohno, S. (1970) Evolution by Gene Duplication, Springer Verlag, New York, NY.Google Scholar
  37. Ohno, S. (1999) The one-to-four rule and paralogues of sex-determining genes. Cell. Mol. Life Sci., 55, 824-830.Google Scholar
  38. Patel, N.H. and Prince, V.E. (2000) Beyond the Hox complex. Genome Biol., 1, 1027.1-1027.4.Google Scholar
  39. Postlethwait, J.H., Woods, I.G., Ngo-Hazelett, P., Yan, Y.-L., Kelly, P.D., Chu, F., Huang, H., Hill-Force, A. and Talbot, W.S. (2000) Zebrafish comparative genomics and the origins of vertebrate chromosomes. Genome Res., 10, 1890-1902.Google Scholar
  40. Robinson-Rechavi, M., Marchand, O., Escriva, H., Bardet, P.-L., Zelus, D., Hughes, S. and Laudet, V. (2001a) Euteleost fish genomes are characterized by expansion of gene families. Genome Res., 11, 781-788.Google Scholar
  41. Robinson-Rechavi, M., Marchand, O., Escriva, H. and Laudet, V. (2001b) An ancestral whole-genome duplication may not have been responsible for the abundance of duplicated fish genes. Curr. Biol., 11, R458-R459.Google Scholar
  42. Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol., 4, 406-425.Google Scholar
  43. Schulte, T., Paschke, K.A., Laessing, U., Lottspeich, F. and Stuermer, C.A. (1997) Reggie-1 and reggie-2, two cell surface proteins expressed by retinal ganglion cells during axon regeneration. Development, 124, 577-587.Google Scholar
  44. Sidow, A. (1996) Gen(om)e duplications in the evolution of early vertebrates. Curr. Opin. Genet. Dev., 6, 715-722Google Scholar
  45. Spring, J. (1997) Vertebrate evolution by interspecific hybridisation-are we polyploid? FEBS Lett., 400, 2-8.Google Scholar
  46. Taylor, J.S. and Brinkmann, H. (2001) 2R or not 2R. Trends Genet., 17, 488-489.Google Scholar
  47. Taylor, J.S., Van de Peer, Y., Braasch, I. and Meyer, A. (2001a) Comparative genomics provides evidence for an ancient genome duplication in fish. Phil. Trans. Roy. Soc. B, 356, 1661-1679.Google Scholar
  48. Taylor, J.S., Van de Peer, Y. and Meyer, A. (2001b) Genome duplication, divergent resolution, and speciation. Trends Genet., 17, 299-301.Google Scholar
  49. X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res., 25, 4876-4882.Google Scholar
  50. Van de Peer, Y., and De Wachter, R. (1994) TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput. Appl. Biosci., 10, 569-570.Google Scholar
  51. Van de Peer, Y., Taylor, J.S., Braasch, I. and Meyer, A. (2001). The ghost of selection past: rates of evolution and functional divergence in anciently duplicated genes. J. Mol. Evol., 53, 434-444.Google Scholar
  52. Van de Peer, Y., Taylor, J.S., Joseph, J. and Meyer, A. (2002a) Wanda: A database of duplicated fish genes. Nucleic Acids Res., 30, 109-112.Google Scholar
  53. Van de Peer, Y., Frickey, T., Taylor, J.S. and Meyer, A. (2002b) Dealing with saturation at the amino acid level: A case study based on anciently duplicated zebrafish genes. Gene, 295,205-211.Google Scholar
  54. Wang, Y. and Gu, X. (2000) Evolution patterns of gene families generated in the early stage of vertebrates. J. Mol. Evol., 51, 88-96.Google Scholar
  55. Wittbrodt, J., Meyer, A. and Schartl, M. (1998) More genes in fish? BioEssays, 20, 511-512.Google Scholar
  56. Woods, I.G., Kelly, P.D., Chu, F., Ngo-Hazelett, P., Yan, Y.-L., Huang, H., Postlethwait, J.H. and Talbot, W.S. (2000) A comparative map of the zebrafish genome. Genome Res., 10, 1903-1914.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Yves Van de Peer
    • 1
  • John S. Taylor
    • 2
  • Axel Meyer
    • 2
  1. 1.Department of Plant Systems Biology, Vlaams Interuniversitair Instituut voor Biotechnologie (VIB)Ghent UniversityGentBelgium
  2. 2.Department of BiologyUniversity of KonstanzKonstanzGermany

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