More genes in vertebrates?

  • Peter W.H. Holland


With the acquisition of complete genome sequences from several animals, there is renewed interest in the pattern of genome evolution on our own lineage. One key question is whether gene number increased during chordate or vertebrate evolution. It is argued here that comparing the total number of genes between a fly, a nematode and human is not appropriate to address this question. Extensive gene loss after duplication is one complication; another is the problem of comparing taxa that are phylogenetically very distant. Amphioxus and tunicates are more appropriate animals for comparison to vertebrates. Comparisons of clustered homeobox genes, where gene loss can be identified, reveals a one to four mode of evolution for Hox and ParaHox genes. Analyses of other gene families in amphioxus and vertebrates confirm that gene duplication was very widespread on the vertebrate lineage. These data confirm that vertebrates have more genes than their closest invertebrate relatives, acquired through gene duplication. abbreviations IHGSC, International Human Genome Sequencing Consortium; TCESC, The C. elegans Sequencing Consortium.

amphioxus evolution gene duplication gene family Hox Parahox 


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  1. Adams, M.D. et al. (2000) The genome sequence of Drosophila melanogaster. Science, 287, 2185-2195.Google Scholar
  2. Aguinaldo, A.M., Turbeville, J.M., Linford, L.S., Rivera, M.C., Garey, J.R., Raff, R. and Lake, J.A. (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature, 387, 489-493.Google Scholar
  3. Arai, R., Suzuki, A. and Akai Y. (1988) The karyotype and DNA value of a cypriniform algae eater, Gyrinocheilus aymonieri. Jpn. J. Ichthyol., 34, 515-517.Google Scholar
  4. Araki, I., Terazawa, K. and Satoh, N. (1996) Duplication of an amphioxus myogenic bHLH gene is independent of vertebrate myogenic bHLH gene duplication. Gene, 171, 231-236.Google Scholar
  5. Aristotle (350 BC) History of Animals (Translation, D'Arcy Wentworth Thompson). Library of the Future, Second Series 1991, World Library, Inc., Garden Grove, CA.Google Scholar
  6. Atkin, N.B. and Ohno, S. (1967) DNA values of four primitive chordates. Chromosoma, 23, 10-13.Google Scholar
  7. Baltimore, D. (2001) Our genome unveiled. Nature, 409, 814-816.Google Scholar
  8. Brooke, N.M., Garcia-Fernàndez, J. and Holland, P.W.H. (1998) The ParaHox gene cluster is an evolutionary sister of the Hox gene cluster. Nature, 392, 920-922.Google Scholar
  9. Claverie, J.-M. (2001) What if there are only 30,000 genes? Science, 291, 1255-1257.Google Scholar
  10. de Rosa, R., Grenier, J.K., Andreeva, T., Cook, C.E., Adoutte, A., Akam, M., Carroll, S.B. and Balavoine, G. (1999) Hox genes in brachiopods and priapulids and protostome evolution. Nature, 399, 772-776.Google Scholar
  11. Ferrier, D.E.K. and Holland, P.W.H. (2001) Ancient origins of the Hox gene cluster. Nature Rev. Genet. 2, 33-38.Google Scholar
  12. Ferrier, D.E.K., Minguillon, C., Holland, P.W.H. and Garcia-Fernandez, J. (2000) The amphioxus Hox cluster: deuterostome posterior flexibility and Hox14. Evol. Dev., 2, 284-293.Google Scholar
  13. Flybase (1999) The Flybase database of the Drosophila genome projects and community literature. Nucleic Acids Res., 27, 85-88.Google Scholar
  14. Furlong, R.F. and Holland, P.W.H. (2002) Were vertebrates octoploid? Phil. Trans. R. Soc. Ser. B, 357, 531-544.Google Scholar
  15. Garcia-Fernández, J. and Holland, P.W.H. (1994) Archetypal organization of the amphioxus Hox gene cluster. Nature 370, 563-566.Google Scholar
  16. Hinegardner, R. and Rosen, D.E. (1972) Cellular DNA content and the evolution of teleostean fishes. Amer. Naturalist, 106, 621-644.Google Scholar
  17. Holland, P.W.H. (1999) Gene duplication: past, present and future. Semin. Cell Dev. Biol., 10, 541-547.Google Scholar
  18. Holland, P.W.H. and Garcia-Fernàndez, J. (1996) Hox genes and chordate evolution. Dev. Biol., 173, 382-395.Google Scholar
  19. Holland, P.W.H., Holland, L.Z., Williams, N.A. and Holland, N.D. (1992) An amphioxus homeobox gene: sequence conservation, spatial expression during development and insights into vertebrate evolution. Development, 116, 653-661.Google Scholar
  20. International Human Genome Sequencing Consortium (2001) Initial sequencing and analysis of the human genome. Nature, 409, 860-921.Google Scholar
  21. Jefferies, R.P.S. and Lewis, D.N. (1978) The English Silurian fossil Placocystites forbesianus and the ancestry of the vertebrates. Phil. Trans. R. Soc. Ser. B, 282, 205-323.Google Scholar
  22. Krakauer, D.C. and Nowak, M. (1999) Evolutionary preservation of redundant duplicated genes. Semin. Cell Dev. Biol., 10, 555-559.Google Scholar
  23. Ohno, S. (1970) Evolution by Gene Duplication, Springer-Verlag, Heidelberg.Google Scholar
  24. Ohno, S. (1999) Gene duplication and the uniqueness of vertebrate genomes circa 1970-1999. Semin. Cell Dev. Biol., 10, 517-522.Google Scholar
  25. Patton, S.J., Luke, G.N. and Holland, P.W.H. (1998) Complex history of a chromosomal paralogy regions: insights from amphioxus aromatic amino acid hydroxylase genes and insulinrelated genes. Mol. Biol. Evol., 15, 1373-1380.Google Scholar
  26. Pendleton, J.W., Nagai, B.K., Murtha, M.T. and Ruddle, F.H. (1993) Expansion of the Hox gene family and the evolution of chordates. Proc. Natl. Acad. Sci. USA, 90, 6300-6304.Google Scholar
  27. Pollard, S.L. and Holland, P.W.H. (2000) Evidence for fourteen homeobox gene clusters in human genome ancestry, Curr. Biol., 10, 1059-1062.Google Scholar
  28. Robinson, E.S., Potter, I.C. and Atkin, N.B. (1975) The nuclear DNA content of lampreys. Experientia, 31, 912-913.Google Scholar
  29. Rubin, G.M. (2001) Comparing species. Nature, 409, 820-821.Google Scholar
  30. Shimeld, S.M. and Holland, P.W.H. (2000) Vertebrate innovations. Proc. Natl. Acad. Sci. USA 97, 4449-4452.Google Scholar
  31. Schmidtke, J., Weiler, C., Kunz, B. and Engel, W. (1977) Isozymes of a tunicate and a cephalochordate as a test of polyploidisation in chordate evolution. Nature, 266, 532-533.Google Scholar
  32. Shu, D.-G., Conway Morris, S. and Zhang, X.-L. (1996) A Pikaialike chordate from the Lower Cambrian of China. Nature, 384, 157-158.Google Scholar
  33. The C. elegans Sequencing Consortium (1998) Genome Sequence of the nematode Caenorhabditis elegans: a platform for investigating biology. Science, 282, 2012-2018.Google Scholar
  34. Venter, J.C., Adams, M.D., Myers, E.W. et al. (2001) The sequence of the human genome. Science, 291, 1304-1351.Google Scholar
  35. Wada, H. and Satoh, N. (1993) Details of the evolutionary history from invertebrates, as deduced from the sequences of 18S rDNA. Proc. Natl. Acad. Sci. USA, 91, 1801-1804.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Peter W.H. Holland
    • 1
  1. 1.School of Animal & Microbial SciencesThe University of Reading, WhiteknightsReadingUnited Kingdom
  2. 2.Department of ZoologyUniversity of OxfordOxfordUnited Kingdom

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