Skip to main content
SpringerLink
Log in

Are all fishes ancient polyploids?

  • Chapter
Book cover Genome Evolution

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • 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.

    PubMed  CAS  Google Scholar 

  • Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389–3402.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Carroll, R.L. (1997) Patterns and Processes of Vertebrate Evolution, Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Gardner, C.A. and Barald, K.F. (1992) Expression patterns of engrailed-like proteins in the chick embryo. Dev. Dyn., 193, 370–388.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Gehring, W.J. (1998). Master Control Genes in Development and Evolution: the Homeobox Story. Yale University Press, New Haven

    Google Scholar 

  • Gibson, T.J. and Spring, J. (1998) Genetic redundancy in vertebrates: polyploidy and persistence of genes encoding multido-main proteins. Trends Genet., 14, 46–49.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Holland, PW. (1997) Vertebrate evolution: something fishy about Hox genes. Curr. Biol., 7, R570–R572.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Holland, P.W. and Garcia-Fernandez, J. (1996) Hox genes and chor-date evolution. Dev. Biol, 173, 382–395.

    Article  PubMed  CAS  Google Scholar 

  • Hughes, A.L. (1994) The evolution of functionally novel proteins after gene duplication. Proc. R. Soc. Lond. B, 256, 119–124.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Lundin, L.-G. (1999) Gene duplications in early metazoan evolution. Cell Dev. Biol, 10, 523–530.

    Article  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • Lynch, M. and Conery, J.S. (2000) The evolutionary fate and consequences of duplicate genes. Science, 290, 1151–1155.

    Article  PubMed  CAS  Google Scholar 

  • Lynch, M. and Force, A. (2000a) The probability of duplicate gene preservation by subfunctionalization. Genetics, 154, 459–473.

    PubMed  CAS  Google Scholar 

  • Lynch, M. and Force, A. (2000b) The origin of interspecific genomic incompatibility via gene duplication. Am. Nat. 156, 590–605.

    Article  Google Scholar 

  • Malaga-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.

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Mellgren E.M. and Johnson, S.L. (2002) The evolution of morphological complexity in zebrafish stripes. Trends Genet., 18, 128–134.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Nelson, J.S. (1994) Fishes of the World, 3rd ed., Wiley, New York, NY

    Google Scholar 

  • Nowak, M.A., Boerlijst, M.C., Cooke, J. and Maynard Smith, J. (1997) Evolution of genetic redundancy. Nature, 388, 167–171.

    Article  PubMed  CAS  Google Scholar 

  • Ohno, S. (1970) Evolution by Gene Duplication, Springer Verlag, New York, NY.

    Google Scholar 

  • Ohno, S. (1999) The one-to-four rule and paralogues of sex-determining genes. Cell. Mol Life Sci., 55, 824–830.

    Article  PubMed  CAS  Google Scholar 

  • Patel, N.H. and Prince, V.E. (2000) Beyond the Hox complex. Genome Biol, 1, 1027.1–1027.4.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol, 4, 406–425.

    PubMed  CAS  Google Scholar 

  • Schulte, T., Paschke, K.A., Laessing, U., Lottspeich, F. and Stu-ermer, C.A. (1997) Reggie-1 and reggie-2, two cell surface proteins expressed by retinal ganglion cells during axon regeneration. Development, 124, 577–587.

    PubMed  CAS  Google Scholar 

  • Sidow, A. (1996) Gen(om)e duplications in the evolution of early vertebrates. Curr. Opin. Genet. Dev., 6, 715–722

    Article  PubMed  CAS  Google Scholar 

  • Spring, J. (1997) Vertebrate evolution by interspecific hybridisation — are we polyploid? FEBS Lett., 400, 2–8.

    Article  PubMed  CAS  Google Scholar 

  • Taylor, J.S. and Brinkmann, H. (2001) 2R or not 2R. Trends Genet., 17, 488–489.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Taylor, J.S., Van de Peer, Y. and Meyer, A. (2001b) Genome duplication, divergent resolution, and speciation. Trends Genet., 17, 299–301.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res., 25, 4876–4882.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 zebraflsh genes. Gene, 295, 205–211.

    Article  PubMed  Google Scholar 

  • Wang, Y. and Gu, X. (2000) Evolution patterns of gene families generated in the early stage of vertebrates. J. Mol. Evol, 51, 88–96.

    PubMed  CAS  Google Scholar 

  • Wittbrodt, J., Meyer, A. and Schartl, M. (1998) More genes in fish? BioEssays, 20, 511–512.

    Article  Google Scholar 

  • 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 zebraflsh genome. Genome Res., 10, 1903–1914.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Author notes

  1. John S. Taylor

    Present address: Department of Biology, University of Victoria, PO Box 3020, Victoria, Canada, V8W 3N5

Authors and Affiliations

  1. Department of Plant Systems Biology, Vlaams Interuniversitair Instituut voor Biotechnologie (VIB), Ghent University, K.L. Ledeganckstraat 35, B-9000, Gent, Belgium

    Yves Van de Peer

  2. Department of Biology, University of Konstanz, D-78457, Konstanz, Germany

    John S. Taylor & Axel Meyer

Authors
  1. Yves Van de Peer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John S. Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Axel Meyer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yves Van de Peer .

Editor information

Editors and Affiliations

  1. University of Konstanz, Germany

    Axel Meyer

  2. Ghent University, Belgium

    Yves Van de Peer

Rights and permissions

Reprints and permissions

Copyright information

© 2003 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Van de Peer, Y., Taylor, J.S., Meyer, A. (2003). Are all fishes ancient polyploids?. In: Meyer, A., Van de Peer, Y. (eds) Genome Evolution. Springer, Dordrecht. https://doi.org/10.1007/978-94-010-0263-9_7

Download citation

  • DOI: https://doi.org/10.1007/978-94-010-0263-9_7

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-3957-4

  • Online ISBN: 978-94-010-0263-9

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation