Skip to main content
PMC home page
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2001 Oct 29;356(1414):1661–1679. doi: 10.1098/rstb.2001.0975

Comparative genomics provides evidence for an ancient genome duplication event in fish.

J S Taylor 1, Y Van de Peer 1, I Braasch 1, A Meyer 1
PMCID: PMC1088543  PMID: 11604130

Abstract

There are approximately 25 000 species in the division Teleostei and most are believed to have arisen during a relatively short period of time ca. 200 Myr ago. The discovery of 'extra' Hox gene clusters in zebrafish (Danio rerio), medaka (Oryzias latipes), and pufferfish (Fugu rubripes), has led to the hypothesis that genome duplication provided the genetic raw material necessary for the teleost radiation. We identified 27 groups of orthologous genes which included one gene from man, mouse and chicken, one or two genes from tetraploid Xenopus and two genes from zebrafish. A genome duplication in the ancestor of teleost fishes is the most parsimonious explanation for the observations that for 15 of these genes, the two zebrafish orthologues are sister sequences in phylogenies that otherwise match the expected organismal tree, the zebrafish gene pairs appear to have been formed at approximately the same time, and are unlinked. Phylogenies of nine genes differ a little from the tree predicted by the fish-specific genome duplication hypothesis: one tree shows a sister sequence relationship for the zebrafish genes but differs slightly from the expected organismal tree and in eight trees, one zebrafish gene is the sister sequence to a clade which includes the second zebrafish gene and orthologues from Xenopus, chicken, mouse and man. For these nine gene trees, deviations from the predictions of the fish-specific genome duplication hypothesis are poorly supported. The two zebrafish orthologues for each of the three remaining genes are tightly linked and are, therefore, unlikely to have been formed during a genome duplication event. We estimated that the unlinked duplicated zebrafish genes are between 300 and 450 Myr. Thus, genome duplication could have provided the genetic raw material for teleost radiation. Alternatively, the loss of different duplicates in different populations (i.e. 'divergent resolution') may have promoted speciation in ancient teleost populations.

Full Text

The Full Text of this article is available as a PDF (233.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Amores A., Force A., Yan Y. L., Joly L., Amemiya C., Fritz A., Ho R. K., Langeland J., Prince V., Wang Y. L. Zebrafish hox clusters and vertebrate genome evolution. Science. 1998 Nov 27;282(5394):1711–1714. doi: 10.1126/science.282.5394.1711. [DOI] [PubMed] [Google Scholar]
  3. Aparicio S. Vertebrate evolution: recent perspectives from fish. Trends Genet. 2000 Feb;16(2):54–56. doi: 10.1016/s0168-9525(99)01934-4. [DOI] [PubMed] [Google Scholar]
  4. Band M. R., Larson J. H., Rebeiz M., Green C. A., Heyen D. W., Donovan J., Windish R., Steining C., Mahyuddin P., Womack J. E. An ordered comparative map of the cattle and human genomes. Genome Res. 2000 Sep;10(9):1359–1368. doi: 10.1101/gr.145900. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barbazuk W. B., Korf I., Kadavi C., Heyen J., Tate S., Wun E., Bedell J. A., McPherson J. D., Johnson S. L. The syntenic relationship of the zebrafish and human genomes. Genome Res. 2000 Sep;10(9):1351–1358. doi: 10.1101/gr.144700. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cantatore P., Roberti M., Pesole G., Ludovico A., Milella F., Gadaleta M. N., Saccone C. Evolutionary analysis of cytochrome b sequences in some Perciformes: evidence for a slower rate of evolution than in mammals. J Mol Evol. 1994 Dec;39(6):589–597. doi: 10.1007/BF00160404. [DOI] [PubMed] [Google Scholar]
  7. Cheng C. H., Chen L. Evolution of an antifreeze glycoprotein. Nature. 1999 Sep 30;401(6752):443–444. doi: 10.1038/46721. [DOI] [PubMed] [Google Scholar]
  8. Dulai K. S., von Dornum M., Mollon J. D., Hunt D. M. The evolution of trichromatic color vision by opsin gene duplication in New World and Old World primates. Genome Res. 1999 Jul;9(7):629–638. [PubMed] [Google Scholar]
  9. Ekker S. C., Ungar A. R., Greenstein P., von Kessler D. P., Porter J. A., Moon R. T., Beachy P. A. Patterning activities of vertebrate hedgehog proteins in the developing eye and brain. Curr Biol. 1995 Aug 1;5(8):944–955. doi: 10.1016/s0960-9822(95)00185-0. [DOI] [PubMed] [Google Scholar]
  10. Elgar G., Clark M. S., Meek S., Smith S., Warner S., Edwards Y. J., Bouchireb N., Cottage A., Yeo G. S., Umrania Y. Generation and analysis of 25 Mb of genomic DNA from the pufferfish Fugu rubripes by sequence scanning. Genome Res. 1999 Oct;9(10):960–971. doi: 10.1101/gr.9.10.960. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fitch W. M. Distinguishing homologous from analogous proteins. Syst Zool. 1970 Jun;19(2):99–113. [PubMed] [Google Scholar]
  12. Force A., Lynch M., Pickett F. B., Amores A., Yan Y. L., Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics. 1999 Apr;151(4):1531–1545. doi: 10.1093/genetics/151.4.1531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gates M. A., Kim L., Egan E. S., Cardozo T., Sirotkin H. I., Dougan S. T., Lashkari D., Abagyan R., Schier A. F., Talbot W. S. A genetic linkage map for zebrafish: comparative analysis and localization of genes and expressed sequences. Genome Res. 1999 Apr;9(4):334–347. [PubMed] [Google Scholar]
  14. Gibson T. J., Spring J. Genetic redundancy in vertebrates: polyploidy and persistence of genes encoding multidomain proteins. Trends Genet. 1998 Feb;14(2):46–50. doi: 10.1016/s0168-9525(97)01367-x. [DOI] [PubMed] [Google Scholar]
  15. Gu X. Early metazoan divergence was about 830 million years ago. J Mol Evol. 1998 Sep;47(3):369–371. doi: 10.1007/pl00013150. [DOI] [PubMed] [Google Scholar]
  16. Holland P. W. The effect of gene duplication on homology. Novartis Found Symp. 1999;222:226–242. [PubMed] [Google Scholar]
  17. Holland P. Homeobox genes in vertebrate evolution. Bioessays. 1992 Apr;14(4):267–273. doi: 10.1002/bies.950140412. [DOI] [PubMed] [Google Scholar]
  18. 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. 1999 May;48(5):565–576. doi: 10.1007/pl00006499. [DOI] [PubMed] [Google Scholar]
  19. Hughes M. K., Hughes A. L. Evolution of duplicate genes in a tetraploid animal, Xenopus laevis. Mol Biol Evol. 1993 Nov;10(6):1360–1369. doi: 10.1093/oxfordjournals.molbev.a040080. [DOI] [PubMed] [Google Scholar]
  20. Kishino H., Hasegawa M. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J Mol Evol. 1989 Aug;29(2):170–179. doi: 10.1007/BF02100115. [DOI] [PubMed] [Google Scholar]
  21. Kumar S., Hedges S. B. A molecular timescale for vertebrate evolution. Nature. 1998 Apr 30;392(6679):917–920. doi: 10.1038/31927. [DOI] [PubMed] [Google Scholar]
  22. Lee M. S. Molecular clock calibrations and metazoan divergence dates. J Mol Evol. 1999 Sep;49(3):385–391. doi: 10.1007/pl00006562. [DOI] [PubMed] [Google Scholar]
  23. Li W. H., Gouy M., Sharp P. M., O'hUigin C., Yang Y. W. Molecular phylogeny of Rodentia, Lagomorpha, Primates, Artiodactyla, and Carnivora and molecular clocks. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6703–6707. doi: 10.1073/pnas.87.17.6703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lundin L. G. Evolution of the vertebrate genome as reflected in paralogous chromosomal regions in man and the house mouse. Genomics. 1993 Apr;16(1):1–19. doi: 10.1006/geno.1993.1133. [DOI] [PubMed] [Google Scholar]
  25. Lundin L. G. Gene duplications in early metazoan evolution. Semin Cell Dev Biol. 1999 Oct;10(5):523–530. doi: 10.1006/scdb.1999.0333. [DOI] [PubMed] [Google Scholar]
  26. Luo J., Zhang Y. P., Zhu C. L., Xiao W. H., Huang S. Y. Genetic diversity in crucian carp (Carassius auratus). Biochem Genet. 1999 Oct;37(9-10):267–279. doi: 10.1023/a:1018751008848. [DOI] [PubMed] [Google Scholar]
  27. Lynch M., Conery J. S. The evolutionary fate and consequences of duplicate genes. Science. 2000 Nov 10;290(5494):1151–1155. doi: 10.1126/science.290.5494.1151. [DOI] [PubMed] [Google Scholar]
  28. Maglott D. R., Katz K. S., Sicotte H., Pruitt K. D. NCBI's LocusLink and RefSeq. Nucleic Acids Res. 2000 Jan 1;28(1):126–128. doi: 10.1093/nar/28.1.126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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. 1999 Dec;11(6):699–704. doi: 10.1016/s0955-0674(99)00039-3. [DOI] [PubMed] [Google Scholar]
  30. Murphy W. J., Sun S., Chen Z., Yuhki N., Hirschmann D., Menotti-Raymond M., O'Brien S. J. A radiation hybrid map of the cat genome: implications for comparative mapping. Genome Res. 2000 May;10(5):691–702. doi: 10.1101/gr.10.5.691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nadeau J. H., Sankoff D. The lengths of undiscovered conserved segments in comparative maps. Mamm Genome. 1998 Jun;9(6):491–495. doi: 10.1007/s003359900806. [DOI] [PubMed] [Google Scholar]
  32. Naruse K., Fukamachi S., Mitani H., Kondo M., Matsuoka T., Kondo S., Hanamura N., Morita Y., Hasegawa K., Nishigaki R. A detailed linkage map of medaka, Oryzias latipes: comparative genomics and genome evolution. Genetics. 2000 Apr;154(4):1773–1784. doi: 10.1093/genetics/154.4.1773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ohno S. The one-to-four rule and paralogues of sex-determining genes. Cell Mol Life Sci. 1999 Jun;55(6-7):824–830. doi: 10.1007/s000180050336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Page R. D. TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci. 1996 Aug;12(4):357–358. doi: 10.1093/bioinformatics/12.4.357. [DOI] [PubMed] [Google Scholar]
  35. Pébusque M. J., Coulier F., Birnbaum D., Pontarotti P. Ancient large-scale genome duplications: phylogenetic and linkage analyses shed light on chordate genome evolution. Mol Biol Evol. 1998 Sep;15(9):1145–1159. doi: 10.1093/oxfordjournals.molbev.a026022. [DOI] [PubMed] [Google Scholar]
  36. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  37. Sharman A. C. Some new terms for duplicated genes. Semin Cell Dev Biol. 1999 Oct;10(5):561–563. doi: 10.1006/scdb.1999.0338. [DOI] [PubMed] [Google Scholar]
  38. Sheppard D. M., Fisher R. A., Lawler S. D., Povey S. Tetraploid conceptus with three paternal contributions. Hum Genet. 1982;62(4):371–374. doi: 10.1007/BF00304561. [DOI] [PubMed] [Google Scholar]
  39. Sidow A. Gen(om)e duplications in the evolution of early vertebrates. Curr Opin Genet Dev. 1996 Dec;6(6):715–722. doi: 10.1016/s0959-437x(96)80026-8. [DOI] [PubMed] [Google Scholar]
  40. Spring J. Vertebrate evolution by interspecific hybridisation--are we polyploid? FEBS Lett. 1997 Jan 2;400(1):2–8. doi: 10.1016/s0014-5793(96)01351-8. [DOI] [PubMed] [Google Scholar]
  41. Stellwag E. J. Hox gene duplication in fish. Semin Cell Dev Biol. 1999 Oct;10(5):531–540. doi: 10.1006/scdb.1999.0334. [DOI] [PubMed] [Google Scholar]
  42. Tajima F., Nei M. Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol. 1984 Apr;1(3):269–285. doi: 10.1093/oxfordjournals.molbev.a040317. [DOI] [PubMed] [Google Scholar]
  43. Taylor J. S., Van de Peer Y., Meyer A. Genome duplication, divergent resolution and speciation. Trends Genet. 2001 Jun;17(6):299–301. doi: 10.1016/s0168-9525(01)02318-6. [DOI] [PubMed] [Google Scholar]
  44. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997 Dec 15;25(24):4876–4882. doi: 10.1093/nar/25.24.4876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Van de Peer Y., De Wachter R. TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci. 1994 Sep;10(5):569–570. doi: 10.1093/bioinformatics/10.5.569. [DOI] [PubMed] [Google Scholar]
  46. Wang Y., Gu X. Evolutionary patterns of gene families generated in the early stage of vertebrates. J Mol Evol. 2000 Jul;51(1):88–96. doi: 10.1007/s002390010069. [DOI] [PubMed] [Google Scholar]
  47. Woods I. G., Kelly P. D., Chu F., Ngo-Hazelett P., Yan Y. L., Huang H., Postlethwait J. H., Talbot W. S. A comparative map of the zebrafish genome. Genome Res. 2000 Dec;10(12):1903–1914. doi: 10.1101/gr.10.12.1903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Zardoya R., Abouheif E., Meyer A. Evolution and orthology of hedgehog genes. Trends Genet. 1996 Dec;12(12):496–497. doi: 10.1016/s0168-9525(96)20014-9. [DOI] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society of London. Series B are provided here courtesy of The Royal Society

RESOURCES