Abstract
The classical (two-round) hypothesis1 of vertebrate genome duplication proposes two successive whole-genome duplication(s) (polyploidizations) predating the origin of fishes, a view now being seriously challenged2,3,4,5,6,7. As the debate largely concerns the relative merits of the 'big-bang mode' theory8,9,10,11,12,13 (large-scale duplication) and the 'continuous mode' theory (constant creation by small-scale duplications)2,3,4,5,6,7,14, we tested whether a significant proportion of paralogous genes in the contemporary human genome was indeed generated in the early stage of vertebrate evolution. After an extensive search of major databases, we dated 1,739 gene duplication events from the phylogenetic analysis of 749 vertebrate gene families. We found a pattern characterized by two waves (I, II) and an ancient component. Wave I represents a recent gene family expansion by tandem or segmental duplications15, whereas wave II, a rapid paralogous gene increase in the early stage of vertebrate evolution, supports the idea of genome duplication(s) (the big-bang mode). Further analysis indicated that large- and small-scale gene duplications both make a significant contribution during the early stage of vertebrate evolution to build the current hierarchy of the human proteome.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Ohno, S. Evolution by Gene Duplication (George Allen and Unwin, London, 1970).
Hughes, A.L. 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 (1999).
Wolfe, K.H. Yesterday's polyploids and the mystery of diploidization. Nature Rev Genet 2, 333–341 (2001).
Meyer, A. & Schartl, M. 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 (1999).
Martin, A. Is tetralogy true? Lack of support for the 'one-to-four rule'. Mol. Biol. Evol. 18, 89–93 (2001).
Lander, E.S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860–921 (2001).
Venter, J.C. et al. The sequence of the human genome. Science 291, 1304–1351 (2001).
Nadeau, J.H. & Sankoff, D. Comparable rates of gene loss and functional divergence after genome duplications early in vertebrate evolution. Genetics 147, 1259–1266 (1997).
Hughes, A.L., da Silva, J . & Friedman, R. Ancient genome duplications did not structure the human Hox-bearing chromosomes. Genome Res. 11, 771–780 (2001).
Schughart, K., Kappen, C. & Ruddle, F.H. Duplication of large genomic regions during the evolution of vertebrate homeobox genes. Proc. Natl Acad. Sci. USA 86, 7067–7071 (1989).
Wang, Y. & Gu, X. Evolutionary patterns of gene families generated in the early stage of vertebrates. J. Mol. Evol. 51, 88–96 (2000).
Lundin, L.G. Evolution of the vertebrate genome as reflected in paralogous chromosomal regions in man and the house mouse. Genomics 16, 1–19 (1993).
Lopreato, G.F. et al. Evolution and divergence of sodium channel genes in vertebrates. Proc. Natl Acad. Sci. USA 98, 7588–7592 (2001).
Spring, J. Vertebrate evolution by interspecific hybridization—are we polyploid? FEBS Lett. 400, 2–8 (1997).
Eichler, E.E. Recent duplication, domain accretion and the dynamic mutation of the human genome. Trends Genet. 17, 661–669 (2001).
Sidow, A. Gen(om)e duplications in the evolution of early vertebrates. Curr. Opin. Genet. Dev. 6, 715–722 (1996).
Li, W.H., Gu, Z., Wang, H. & Nekrutenko, A. Evolutionary analyses of the human genome. Nature 409, 847–849 (2001).
Nei, M., Gu, X. & Stinikova, T. Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc. Natl Acad. Sci. USA. 94, 7799–7806 (1997).
McLysaght, A., Hokamp, K. & Wolfe, K.H. Extensive genomic duplication during early chordate evolution. Nature Genet. 31, 200–204 (2002); advance online publication, 28 May 2002 (DOI:10.1038/ng884).
Fishman, M.C. Genomics. Zebrafish—the canonical vertebrate. Science 294, 1290–1291 (2001).
Iwabe, N., Kuma, K. & Miyata, T. Evolution of gene families and relationship with organismal evolution: rapid divergence of tissue-specific genes in the early evolution of chordates. Mol. Biol. Evol. 13, 483–493 (1996).
Nikoh, N. et al. An estimate of divergence time of Parazoa and Eumetazoa and that of Cephalochordata and Vertebrata by aldolase and triose phosphate isomerase clocks. J. Mol. Evol. 45, 97–106 (1997).
Lynch, M. & Conery, J.S. The evolutionary fate and consequences of duplicate genes. Science 290, 1151–1155 (2000).
Thompson, J.D., Higgins, D.G. & Gibson, T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994).
Saitou, N. & Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425 (1987).
Gu, X. Early metazoan divergence was about 830 million years ago. J. Mol. Evol. 47, 369–371 (1998).
Kumar, S. & Hedges, S.B. A molecular timescale for vertebrate evolution. Nature 392, 917–920 (1998).
Nei, M., Xu, P. & Glazko, G. Estimation of divergence times from multiprotein sequences for a few mammalian species and several distantly related organisms. Proc. Natl Acad. Sci. USA 98, 2497–2502 (2001).
Takezaki, N., Rzhetsky, A. & Nei, M. Phylogenetic test of the molecular clock and linearized trees. Mol. Biol. Evol. 12, 823–833 (1995).
Long, M. et al. Gene duplication and evolution [Technical Comments]. Science 293, 1551 (2001).
Acknowledgements
We thank W.H. Li and W. Nordstrom for their comments. This study is supported by an NIH grant to X.G. X.G. is the 2001 DuPont Young Professor.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Rights and permissions
About this article
Cite this article
Gu, X., Wang, Y. & Gu, J. Age distribution of human gene families shows significant roles of both large- and small-scale duplications in vertebrate evolution. Nat Genet 31, 205–209 (2002). https://doi.org/10.1038/ng902
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ng902
This article is cited by
-
Recent genome duplications facilitate the phenotypic diversity of Hb repertoire in the Cyprinidae
Science China Life Sciences (2021)
-
Co-expression network analysis of duplicate genes in maize (Zea mays L.) reveals no subgenome bias
BMC Genomics (2016)
-
Age distribution patterns of human gene families: divergent for Gene Ontology categories and concordant between different subcellular localizations
Molecular Genetics and Genomics (2014)
-
Evolution of the Cdk-activator Speedy/RINGO in vertebrates
Cellular and Molecular Life Sciences (2012)
-
Large Scale of Human Duplicate Genes Divergence
Journal of Molecular Evolution (2012)