Journal of Molecular Evolution

, Volume 59, Issue 2, pp 190–203 | Cite as

Phylogenetic Timing of the Fish-Specific Genome Duplication Correlates with the Diversification of Teleost Fish

  • Simone Hoegg
  • Henner Brinkmann
  • John S. Taylor
  • Axel MeyerEmail author


For many genes, ray-finned fish (Actinopterygii) have two paralogous copies, where only one ortholog is present in tetrapods. The discovery of an additional, almost-complete set of Hox clusters in teleosts (zebrafish, pufferfish, medaka, and cichlid) but not in basal actinopterygian lineages (Polypterus) led to the formulation of the fish-specific genome duplication hypothesis. The phylogenetic timing of this genome duplication during the evolution of ray-finned fish is unknown, since only a few species of basal fish lineages have been investigated so far. In this study, three nuclear genes (fzd8, sox11, tyrosinase) were sequenced from sturgeons (Acipenseriformes), gars (Semionotiformes), bony tongues (Osteoglossomorpha), and a tenpounder (Elopomorpha). For these three genes, two copies have been described previously teleosts (e.g., zebrafish, pufferfish), but only one orthologous copy is found in tetrapods. Individual gene trees for these three genes and a concatenated dataset support the hypothesis that the fish-specific genome duplication event took place after the split of the Acipenseriformes and the Semionotiformes from the lineage leading to teleost fish but before the divergence of Osteoglossiformes. If these three genes were duplicated during the proposed fish-specific genome duplication event, then this event separates the species-poor early-branching lineages from the species-rich teleost lineage. The additional number of genes resulting from this event might have facilitated the evolutionary radiation and the phenotypic diversification of the teleost fish.


Genome duplication Gene duplication Actinopterygii sox fzd tyrosinase 



We thank members of the Meyer lab, in particular, Yves Van de Peer and Walter Salzburger, for discussion. This work was supported by the University of Konstanz and by grants from the Deutsche Forschungsgemeinschaft and the Fond der Chemischen Industrie to A.M.


  1. Acampora, D, D’Esposito, M, Faiella, A, Pannese, M, Migliaccio, E, Morelli, F, Stornaiuolo, A, Nigro, V, Simeone, A, Boncinelli, E 1989The human HOX gene familyNucleic Acids Res171038510402PubMedGoogle Scholar
  2. Amores, A, Force, A, Yan, YL, Joly, L, Amemiya, C, Fritz, A, Ho, RK, Langeland, J, Prince, V, Wang, YL, Westerfield, M, Ekker, M, Postlethwait, JH 1998Zebrafish hox clusters and vertebrate genome evolutionScience28217111714PubMedGoogle Scholar
  3. Amores, A, Suzuki, T, Yan, Y, Pomeroy, J, Singer, A, Amemiya, C, Postlethwait, JH 2004Developmental roles of pufferfish Hox clusters and genome evolution in ray-fin fishGenome Res14110PubMedGoogle Scholar
  4. Aparicio, S, Chapman, J, Stupka, E, Putnam, N, Chia, Jm, Dehal, P, Christoffels, A, Rash, S, Hoon, S, Smit, A, Gelpke, MDS, Roach, J, Oh, T, Ho, IY, Wong, M, Detter, C, Verhoef, F, Predki, P, Tay, A, Lucas, S, Richardson, P, Smith, SF, Clark, MS, Edwards, YJK, Doggett, N, Zharkikh, A, Tavtigian, SV, Pruss, D, Barnstead, M, Evans, C, Baden, H, Powell, J, Glusman, G, Rowen, L, Hood, L, Tan, YH, Elgar, G, Hawkins, T, Venkatesh, B, Rokhsar, D, Brenner, S 2002Whole-genome shotgun assembly and analysis of the genome of Fugu rubripesScience29713011310CrossRefPubMedGoogle Scholar
  5. Arratia, G 2001The sister-group of Teleostei: Consensus and disagreementsJ Vert Paleontol21767772Google Scholar
  6. Barnes, WM 1994PCR amplification of up to 35-kb DNA with high fidelity and high yield from λ bacteriophage templatesProc Natl Acad Sci USA9122162220PubMedGoogle Scholar
  7. Barbazuk, BB, Korf, I, Kadavi, C, Heyen, J, Tate, S, Wun, E, Bedell, JA, McPherson, JD, Johnson, SL 2000The syntenic relationship of the zebrafish and human genomesGenome Res1013511358CrossRefPubMedGoogle Scholar
  8. Bowles, J, Schepers, G, Koopman, P 2000Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicatorsDev Biol227239255PubMedGoogle Scholar
  9. Camp, E, Lardelli, M 2001Tyrosinase gene expression in zebrafish embryosDev Genes Evol211150153CrossRefPubMedGoogle Scholar
  10. Chiang, EFL, Pai, C-I, Wyatt, M, Yan, Y, Postlethwait, J, Chung, B 2001Two Sox9 Genes on Duplicated Zebrafish Chromosomes: Expression of similar transcription activators in distinct sitesDev Biol231149163PubMedGoogle Scholar
  11. Eldredge, N, Stanley, SM 1984Living fossilsSpringer-VerlagNew YorkGoogle Scholar
  12. Force, A, Lynch, M, Pickett, FB, Amores, A, Yan, Y, Postlethwait, J 1999Preservation of duplicate genes by complementary, degenerative mutationsGenetics15115311545PubMedGoogle Scholar
  13. Garcia-Fernandez, J, Holland, PW 1994Archetypal organization of the amphioxus Hox gene clusterNature370563566PubMedGoogle Scholar
  14. Gates, MA, Kim, L, Egan, ES, Cardozo, T, Sirotkin, HI, Dougan, ST, Lashkari, D, Abagyan, R, Schier, AF, Talbot, WS 1999A genetic linkage map for zebrafish: Comparative analysis and localization of genes and expressed sequencesGenome Res9334347PubMedGoogle Scholar
  15. Giebel, LB, Tripathi, RK, Strunk, KM, Hanifin, JM, Jackson, CE, King, RA, Spritz, RA 1991Tyrosinase gene mutations associated with type IB ( “yellow”) oculocutaneous albinismAm J Hum Genet4811591167PubMedGoogle Scholar
  16. Graham, A, Papalopulu, N, Krumlauf, R 1989The murine and Drosophila homeobox gene complexes have common features of organization and expressionCell57367378PubMedGoogle Scholar
  17. Grande, L, Bemis, WE 1996Interrelationships of Acipenseriformes, with comments on “Chondrostei.”Stiassny, MLJParenti, LRJohnson, GD eds. Interrelationships of fishesAcademic PressLondon85115Google Scholar
  18. Harvey, RP, Tabin, CJ, Melton, DA 1986Embryonic expression and nuclear localization of Xenopus homeobox (Xhox) gene productsEMBO J512371244PubMedGoogle Scholar
  19. Hedges, SB, Kumar, S 2003Genomic clocks and evolutionary timescalesTrends Genet19200206PubMedGoogle Scholar
  20. Huelsenbeck, JP, Ronquist, F 2001MRBAYES: Bayesian inference of phylogenetic treesBioinformatics17754755Google Scholar
  21. Inagaki, H, Bessho, Y, Koga, A, Hori, H 1994Expression of the tyrosinase-encoding gene in a colorless melanophore mutant of the medaka fish, Oryzias latipesGene15319324Google Scholar
  22. Inoue, JG, Miya, M, Tsukamoto, K, Nishida, M 2001A mitogenomic perspective on the basal teleostean phylogeny: Resolving higher-level relationships with longer DNA sequencesMol Phylogenet Evol20275285PubMedGoogle Scholar
  23. Inoue, JG, Miya, M, Tsukamoto, K, Nishida, M 2003Basal actinopterygian relationships: A mitogenomic perspective on the phylogeny of the “ancient fish.”Mol Phylogenet Evol26110120PubMedGoogle Scholar
  24. Kao, H, Lee, S-C 2002Phosphoglucose isomerases of hagfish, zebrafish, gray mullet, toad, and snake, with reference to the evolution of the genes in vertebratesMol Biol Evol19367374PubMedGoogle Scholar
  25. Kishino, H, Hasegawa, M 1989Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoideaJ Mol Evol29170179PubMedGoogle Scholar
  26. Kumar, S, Hedges, SB 1998A molecular timescale for vertebrate evolutionNature392917920CrossRefPubMedGoogle Scholar
  27. Kumar, S, Tamura, K, Jakobsen, IB, Nei, M 2001MEGA2: molecular evolutionary genetics analysis softwareBioinformatics1712441245CrossRefPubMedGoogle Scholar
  28. Kumazawa, Y, Nishida, M 2000Molecular phylogeny of osteoglossoids: A new model for Gondwanian origin and plate tectonic transportation of the Asian arowanaMol Biol Evol1718691878PubMedGoogle Scholar
  29. Kumazawa, Y, Yamaguchi, M, Nishida, M 1999Mitochondrial molecular clocks and the origin of euteleostean biodiversity: Familial radiation of Perciforms may have predated the Cretaceous/Tertiary boundaryKato, M eds. The biology of biodiversitySpringer-VerlagHong Kong3552Google Scholar
  30. Le, HL, Lecointre, G, Perasso, R 1993A 28S rRNA-based phylogeny of the gnathostomes: First steps in the analysis of conflict and congruence with morphologically based cladogramsMol Phylogenet Evol23151PubMedGoogle Scholar
  31. Lecointre, G, Philippe, H, Le, HL, Le Guyader, H 1994How many nucleotides are required to resolve a phylogenetic problem? The use of a new statistical method applicable to available sequencesMol Phylogenet Evol3292309PubMedGoogle Scholar
  32. Li, WH 1980Rate of gene silencing at duplicate loci: A theoretical study and interpretation of data from tetraploid fishesGenetics95237258PubMedGoogle Scholar
  33. Lister, JA, Close, J, Raible, DW 2001Duplicate mitf genes in zebrafish: Complementary expression and conservation of melanogenic potentialDev Biol237333344CrossRefPubMedGoogle Scholar
  34. Lynch, M 2002Gene duplication and evolutionScience297945947PubMedGoogle Scholar
  35. Lynch, M, Force, A 2000aThe probability of duplicate gene preservation by subfunctionalizationGenetics154459473Google Scholar
  36. Lynch, M, Force, A 2000bThe origin of interspecific genomic incompatibility via gene duplicationAm Nat156590605Google Scholar
  37. Lynch, M, Conery, JS 2000The evolutionary fate and consequences of duplicate genesScience29011511155CrossRefPubMedGoogle Scholar
  38. Lynch, M, Conery, JS 2003The evolutionary demography of duplicate genesJ Struct Funct Genomics33544CrossRefPubMedGoogle Scholar
  39. Málaga-Trillo, E, Meyer, A 2001Genome duplications and accelerated evolution of Hox genes and cluster architecture in teleost fishesAm Zool41676686Google Scholar
  40. Martinez-Barbera, JP, Toresson, H, Da Rocha, S, Krauss, S 1997Cloning and expression of three members of the zebrafish Bmp family: Bmp2a, Bmp2b and Bmp4Gene1985359PubMedGoogle Scholar
  41. Merritt, TJS, Quattro, JM 2001Evidence for a period of directional selection following gene duplication in a neurally expressed locus of triosephosphate isomeraseGenetics159689697PubMedGoogle Scholar
  42. Meyer, A, Schartl, M 1999Gene and genome duplications in vertebrates: The one-to-four (-to-eight in fish) rule and the evolution of novel gene functionsCurr Opin Cell Biol11699704CrossRefPubMedGoogle Scholar
  43. Meyer, AVan de Peer, Y eds. 2003Genome evolution: Gene and genome duplications and the origin of novel gene functionsKluwer AcademicDordrechtGoogle Scholar
  44. Meyer, A, Zardoya, R 2003Recent advances in the (molecular) phylogeny of vertebratesAnnu Rev Ecol Syst34311338CrossRefPubMedGoogle Scholar
  45. Miya, M, Nishida, M 2000Use of mitogenomic information in teleostean molecular phylogenetics: A tree-based exploration under the maximum-parsimony optimality criterionMol Phylogenet Evol17437455CrossRefPubMedGoogle Scholar
  46. Miya, M, Takeshima, H, Endo, H, Ishiguro, NB, Inoue, JG, Mukai, T, Satoh, TP, Yamaguchi, M, Kawaguchi, A, Mabuchi, K, Shirai, SM, Nishida, M 2003Major patterns of higher teleostean phylogenies: A new perspective based on 100 complete mitochondrial DNA sequencesMol Phylogenet Evol26121138CrossRefPubMedGoogle Scholar
  47. 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, Shima, A 2000A detailed linkage map of medaka, Oryzias latipes: Comparative genomics and genome evolutionGenetics15417731784PubMedGoogle Scholar
  48. Nei, M, Xu, P, Glazko, G 2001Estimation of divergence times from multiprotein sequences for a few mammalian species and several distantly related organismsProc Natl Acad Sci USA9824972502CrossRefPubMedGoogle Scholar
  49. Nelson, J 1994Fishes of the worldWileyNew YorkGoogle Scholar
  50. Noack, K, Zardoya, R, Meyer, A 1996The complete mitochondrial DNA sequence of the bichir (Polypterus ornatipinnis), a basal ray-finned fish: Ancient establishment of the consensus vertebrate gene orderGenetics14411651180PubMedGoogle Scholar
  51. Normark, BB, McCune, AR, Harrison, RG 1991Phylogenetic relationships of neopterygian fishes, inferred from mitochondrial DNA sequencesMol Biol Evol8819834PubMedGoogle Scholar
  52. Ohno, S 1970Evolution by gene duplicationSpringer-VerlagNew YorkGoogle Scholar
  53. Ohno, S 1999Gene duplication and the uniqueness of vertebrate genomes circa 1970–1999Semin Cell Dev Biol10517522PubMedGoogle Scholar
  54. Patterson, C 1973Interrelationships of holosteansGreenwood, HMiles, RSPatterson, C eds. Interrelationships of fishesZool J Linn Soc LondSuppl 1233305Google Scholar
  55. Philippe, H 1993MUST, a computer package of Management Utilities for Sequences and TreesNucleic Acids Res2152645272PubMedGoogle Scholar
  56. Postlethwait, JH, Woods, IG, Ngo-Hazelett, P, Yan, Y-L, Kelly, PD, Chu, F, Huang, H, Hill-Force, A, Talbot, WS 2000Zebrafish comparative genomics and the origins of vertebrate chromosomesGenome Res1018901902PubMedGoogle Scholar
  57. Rimini, R, Beltrame, M, Argenton, F, Szymczak, D, Cotelli, F, Bianchi, ME 1999Expression patterns of zebrafish sox11A, sox11B and sox21Mech Dev89167171PubMedGoogle Scholar
  58. Risinger, C, Salaneck, E, Soderberg, C, Gates, M, Postlethwait, JH, Larhammar, D 1998Cloning of two loci for synapse protein Snap25 in zebrafish: comparison of paralogous linkage groups suggests loss of one locus in the mammalian lineageJ Neurosci Res54563573PubMedGoogle Scholar
  59. Robinson-Rechavi, M, Marchand, O, Escriva, H, Laudet, V 2001An ancestral whole-genome duplication may not have been responsible for the abundance of duplicated fish genesCurr Biol11R458R459PubMedGoogle Scholar
  60. Rodríguez, FJ, Oliver, A, Marìn, A, Medina, JR 1990The general stochastic model of nucleotide substitutionJ Theor Biol142485501PubMedGoogle Scholar
  61. Sambrook, J, Fritsch, EF, Maniatis, T 1989Molecular cloning—A laboratory manualCold Spring Harbor Laboratory PressCold Spring Harbor, NYGoogle Scholar
  62. Schmidt, HA, Strimmer, K, Vingron, M, Haeseler, A 2002TREE-PUZZLE: Maximum likelihood phylogenetic analysis using quartets and parallel computingBioinformatics18502504CrossRefPubMedGoogle Scholar
  63. Schultze, HP, Wiley, , EO,  1984The neopterygian Amia as a living fossilEldredge, NStanley, SM eds. Living fossilsSpringer-VerlagNew York153159Google Scholar
  64. Shimodaira, H 2002An approximately unbiased test of phylogenetic tree selectionSyst Biol51492508CrossRefPubMedGoogle Scholar
  65. Shimodaira, H, Hasegawa, M 1999Multiple comparisons of log-likelihoods with applications to phylogenetic inferenceMol Biol Evol1611141116Google Scholar
  66. Sidow, A 1996Gen(om)e duplications in the evolution of early vertebratesCurr Opin Genet Dev6715722PubMedGoogle Scholar
  67. Spring, J 1997Vertebrate evolution by interspecific hybridisation—Are we polyploid?FEBS Lett40028PubMedGoogle Scholar
  68. Strimmer, K, Rambaut, A 2002Inferring confidence sets of possibly misspecified gene treesProc R Soc Lond B Biol Sci269137142PubMedGoogle Scholar
  69. Taylor, JS, Peer, Y, Braasch, I, Meyer, A 2001aComparative genomics provides evidence for an ancient genome duplication event in fishPhilos Trans R Soc Lond B Biol Sci35616611679Google Scholar
  70. Taylor, JS, Peer, Y, Meyer, A 2001bRevisiting a recent test of the ancient fish-specific genome duplication hypothesisCurr Biol11R1005R1007Google Scholar
  71. Taylor, JS, Peer, Y, Meyer, A 2001cGenome duplication, divergent resolution and speciationTrends Genet17299301Google Scholar
  72. Taylor, JS, Braasch, I, Frickey, T, Meyer, A, Peer, Y 2003Genome duplication, a trait shared by 22,000 species of ray-finned fishGenome Res13382390PubMedGoogle Scholar
  73. Thompson, JD, Gibson, TJ, Plewniak, F, Jeanmougin, F, Higgins, DG 1997The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis toolsNucleic Acids Res2548764882CrossRefPubMedGoogle Scholar
  74. Peer, Y, Taylor, JS, Braasch, I, Meyer, A 2001The ghost of selection past: Rates of evolution and functional divergence of anciently duplicated genesJ Mol Evol53436446PubMedGoogle Scholar
  75. Peer, Y, Frickey, T, Taylor, JS, Meyer, A 2002aDealing with saturation at the amino acid level: a case study based on anciently duplicated zebrafish genesGene295205211Google Scholar
  76. Peer, Y, Taylor, JS, Jayabalan, J, Meyer, A 2002bWanda: A data base of duplicated fish genesNucleic Acids Res30109112Google Scholar
  77. Van de Poele, K, Vos, W, Taylor, JS, Meyer, A, Peer, Y 2004Major events in the genome evolution of vertebrates: Paranome age and size differs considerably between ray-finned fishes and land vertebratesProc Natl Acad Sci USA10116381643PubMedGoogle Scholar
  78. Wang, Y, Macke, JP, Abella, BS, Andreasson, K, Worley, P, Gilbert, DJ, Copeland, NG, Jenkins, NA, Nathans, J 1996A large family of putative transmembrane receptors homologous to the product of the Drosophila tissue polarity Gene frizzledJ Biol Chem27144684476PubMedGoogle Scholar
  79. Wiley, EO, Schultze, HP 1984Family Lepisosteidae (gars) as living fossilsEldredge, NStanley, SM eds. Living fossilsSpringer-VerlagNew York160165Google Scholar
  80. Wittbrodt, J, Meyer, A, Schartl, M 1998More genes in fish?BioEssays20511515Google Scholar
  81. Yang, Z 1997PAML: Program package for phylogenetic analysis by maximum likelihoodCABIOS13555556PubMedGoogle Scholar
  82. Zardoya, R, Meyer, A 2001Vertebrate phylogeny: limits of inference of mitochondrial genome and nuclear rRNA sequence data due to an adverse phylogenetic signal/homoplasy ratioAhlberg, P eds. Major events in early vertebrate evolution: Palaeontology phylogeny and developmentTaylor and FrancisLondon135155Google Scholar
  83. Zwickl, DJ, Hillis, DM 2002Increased taxon sampling greatly reduces phylogenetic errorSyst Biol51588598PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Simone Hoegg
    • 1
  • Henner Brinkmann
    • 1
    • 2
  • John S. Taylor
    • 1
    • 3
  • Axel Meyer
    • 1
    Email author
  1. 1.Department of BiologyUniversity of KonstanzKonstanzGermany
  2. 2.Département de biochimieUniversité de MontrealMontrealCanada
  3. 3.Department of BiologyUniversity of VictoriaVictoriaCanada

Personalised recommendations