, Volume 127, Issue 1–3, pp 321–327 | Cite as

Phylogenetic conservation of chromosome numbers in Actinopterygiian fishes



The genomes of ray-finned fishes (Actinopterygii) are well known for their evolutionary dynamism as reflected by drastic alterations in DNA content often via regional and whole-genome duplications, differential patterns of gene silencing or loss, shifts in the insertion-to-deletion ratios of genomic segments, and major re-patternings of chromosomes via non-homologous recombination. In sharp contrast, chromosome numbers in somatic karyotypes have been highly conserved over vast evolutionary timescales – a histogram of available counts is strongly leptokurtic with more than 50% of surveyed species displaying either 48 or 50 chromosomes. Here we employ comparative phylogenetic analyses to examine the evolutionary history of alterations in fish chromosome numbers. The most parsimonious ancestral state for major actinopterygiian clades is 48 chromosomes. When interpreted in a phylogenetic context, chromosome numbers evidence many recent instances of polyploidization in various lineages but there is no clear indication of a singular polyploidization event that has been hypothesized to have immediately preceded the teleost radiation. After factoring out evident polyploidizations, a correlation between chromosome numbers and genome sizes across the Actinopterygii is marginally statistically significant (p = 0.012) but exceedingly weak (R 2 = 0.0096). Overall, our phylogenetic analysis indicates a mosaic evolutionary pattern in which the forces that govern labile features of fish genomes must operate largely independently of those that operate to conserve chromosome numbers.


chromosome evolution comparative method fish karyotypes genome size polyploidization 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Allendorf, F.W., Thorgaard, G.H. 1984

    Tetraploidy and the evolution of Salmonid fishes

    Turner, B.J. eds. Evolutionary Genetics of FishesPlenum PressNew York153
    Google Scholar
  2. Amores, A., Suzuki, T., Yan, Y.L., Pomeroy, J., Singer, A., Amemiya,  C., Postlethwait, J.H. 2004Developmental roles of pufferfish Hox clusters and genome evolution in ray-finned fishGenome Res.14110PubMedCrossRefGoogle Scholar
  3. Aparicio, S., Chapman, J., Stupka, E., Putnam, N., Chia, J., Dehal, P., Christoffels, A., Rash, S., Hoon, S., Smit, A., Gelpke, M.D.S., Roach, J., Oh, T., Ho, I.Y., Wong, M., Detter,  C., Verhoef, F., Predki, P., Tay, A., Lucas, S., Richardson,  P., Smith, S.F., Clark, M.S., Edwards, Y.J.K., Doggett, N., Zharkikh, A., Tavtigian, S.V., Pruss, D., Barnstead, M., Evans, C., Baden, H., Powell, J., Glusman, G., Rowen, L., Hood, L., Tan, Y.H., Elgar, G., Hawkins, T., Venkatesh, B., Rokhsar, D., Brenner, S. 2002Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes Science29713011310PubMedCrossRefGoogle Scholar
  4. Arkhipchuk, V.V. 1995Role of chromosomal and genome mutations in the evolution of bony fishesHydrobiologia315565Google Scholar
  5. Blomberg, S.P., Garland, T. 2002Tempo and mode in evolution: phylogenetic inertia, adaptation, and comparative methodsJ. Evolution. Biol.15899910CrossRefGoogle Scholar
  6. Christoffels, A., Koh, E.G.L., Chia, J.-M., Brenner, S., Aparicio, S., Venkatesh, B. 2004Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishesMol. Biol. Evolution2111461151CrossRefGoogle Scholar
  7. Almeida-Toledo, L.F., Daniel-Silva, M.F.Z., Moyses, C.B., Fonteles, S.B.A., Lopes, C.E., Akama, A., Foresti, F. 2002Chromosome evolution in a fish: sex chromosome variability in Eigenmannia virescens (Gymnotiformes: Sternopygidae)Cytogen. Genome Res.99164169CrossRefGoogle Scholar
  8. Devlin, R.H., Nagahama, Y. 2002Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influencesAquaculture208191364CrossRefGoogle Scholar
  9. Ferris, S.D. 1984

    Tetraploidy and the evolution of catostomid fishes

    Turner, B.J. eds. Evolutionary Genetics of FishPlenum PressNew York
    Google Scholar
  10. Force, A., Lynch, M., Pickett, F.B., Amores, A., Yan, Y.L., Postlethwait,  J. 1999Preservation of duplicate genes by complementary, degenerative mutationsGenetics15115311545PubMedGoogle Scholar
  11. Gregory, T.R., 2005. Animal Genome Size Database.
  12. Hinegardner, R. 1976

    Evolution of genome size

    Ayala, F.J. eds. Molecular EvolutionSinauerSunderland179199
    Google Scholar
  13. Hinegardner, R., Rosen, D.E. 1972Cellular DNA content and the evolution of teleostean fishesAm. Naturalist106621644CrossRefGoogle Scholar
  14. Holland, P.W., J. Garcia-Fernandez, J.W. Williams & A. Sidow, 1994. Gene duplications and the origins of vertebrate development. Development supplement: 125–133Google Scholar
  15. Jaillon, O., Aury, J.M., Brunet, F., Petit, J.L., Stange-Thomann, N., Mauceli, E., Bouneau, L., Fischer, C., Ozouf-Costaz, C., Bernot, A., Nicaud, S., Jaffe, D., Fisher, S., Lutfalla,  G., Dossat, C., Segurens, B., Dasilva, C., Salanoubat,  M., Levy, M., Boudet, N., Castellano, S., Anthouard,  R., Jubin, C., Castelli, V., Katinka, M., Vacherie,  B., Biemont, C., Skalli, Z., Cattolico, L., Poulain, J., Berardinis, V., Cruaud, C., Duprat, S., Brottier, P., Coutanceau,  J.P., Gouzy, J., Parra, G., Lardier, G., Chapple,  C., McKernan, K.J., McEwan, P., Bosak, S., Kellis,  M., Volff, J.-N., Guigo, R., Zody, M.C., Mesirov, J., Lindblad-Toh, K., Birren, B., Nusbaum, C., Kahn, D., Robinson-Rechavi,  M., Laudet, V., Schachter, V., Quetier, F., Saurin, W., Scarpelli, C., Wincker, P., Lander, E.S., Weissenbach,  J., Crollius, H.R. 2004Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotypeNature431946957PubMedCrossRefGoogle Scholar
  16. Kawakami, K., Noda, T. 2004Transposition of the Tol2 element, an Ac-like element from the Japanese medaka fish Oryzias latipes, in mouse embryonic stem cellsGenetics166895899PubMedCrossRefGoogle Scholar
  17. Kawakami, K., Shima, A., Kawakami, N. 2000Identification of a functional transposase of the Tol2 element, an Ac-like element from the Japanese medaka fish, and its transposition in the zebrafish germ lineageProc. Natl. Acad. Sci. USA971140311408PubMedCrossRefGoogle Scholar
  18. Larhammar, D., Risinger, C. 1994Molecular genetic aspects of tetraploidy in the common carp, Cyprinus carpio Mol. Phylogenet. Evol.35968PubMedCrossRefGoogle Scholar
  19. Maddison, D.R., Maddison, W.P. 2000MacClade 4: Analysis of Phylogeny and Character EvolutionSinauerSunderland, MAGoogle Scholar
  20. Mank, J.E. & J.C. Avise, in press. Cladogenetic correlates of genomic expansions in the recent evolution of actinopterygiian fishes. Proc. Roy. Soc. London B 273: 33–38Google Scholar
  21. Mank, J.E., D.E.L. Promislow & J.C. Avise, 2006. Evolution of alternative sex determining mechanisms in teleost fishes. Biol. J. Linnean Soc. 87: 83–93Google Scholar
  22. Mank, J.E., Promislow, D.E.L., Avise, J.C. 2005Phylogenetic perspectives on the evolution of parental care in fishesEvolution5915701578PubMedCrossRefGoogle Scholar
  23. Meyer, A., Malaga-Trillo, E. 1999Vertebrate genomics: more fishy tales about Hox genesCurr. Biol.9r210r213PubMedCrossRefGoogle Scholar
  24. 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 Biol.11699704PubMedCrossRefGoogle Scholar
  25. Navarro, A., Barton, N.H. 2003aAccumulating postzygotic isolation gene in parapatry: a new twist on chromosomal speciationEvolution57447459CrossRefGoogle Scholar
  26. Navarro, A., Barton, N.H. 2003bChromosomal speciation and molecular divergence – accelerated evolution in rearranged chromosomesScience300321324CrossRefGoogle Scholar
  27. Neafsey, D.E., Palumbi, S.R. 2003Genome size evolution in pufferfish: a comparative analysis of diodontid and tetraodontid pufferfish genomesGenome Res.13821839PubMedCrossRefGoogle Scholar
  28. Ohno, S. 1967Sex Chromosomes and Sex-Linked GenesSpringer-VerlagNew YorkGoogle Scholar
  29. Ozouf-Costaz, C., Brandt, J., Korting, C., Pisano, E., Bonillo, C., Coutanceau, J.P., Volff, J.-N. 2004Genome dynamics and chromosomal localization of the non-LTR retrotransposons Rex1 and Rex3 in Antarctic fishAntarctic Sci.165157CrossRefGoogle Scholar
  30. Postlethwait, J.H., Woods, I.G., Ngo-Hazelett, P., Yan, Y.L., Kelly, P.D., Chu, F., Huang, H., Hill-Force, A., Talbot, W.S. 2002Zebrafish comparative genomics and the origins of vertebrate chromosomesGenome Res.1018901902CrossRefGoogle Scholar
  31. Robinson-Rechavi, M., Laudet, V. 2001Evolutionary rates of duplicate genes in fish and mammalsMol. Biol. Evol.18681683PubMedGoogle Scholar
  32. Robinson-Rechavi, M., Marchand, O., Schriva, H., Bardet, P.L., Zelus, D., Hughes, S., Laudet, V. 2001Euteleost fish genomes are characterized by expansions of gene familiesGenome Res.11781788PubMedCrossRefGoogle Scholar
  33. Smith, S.F., Snell, P., Gruetzner, F., Bench, A.J., Haaf, T., Metcalfe, J.A., Green, A.R., Elgar, G. 2002Analysis of the extent of shared synteny and conserved gene orders between the genome of Fugu rupripes and human 20qGenome Res.12776784PubMedCrossRefGoogle Scholar
  34. Sokal, R.R., Rohlf, F.J. 1995Biometry: The Principle and Practice of Statistics in Biology ResearchFreemand and CoNew YorkGoogle Scholar
  35. Stephens, S.G. 1951Possible significance of duplications in evolutionAdv. Genet.4247265PubMedCrossRefGoogle Scholar
  36. Thomas, J.W., Touchman, J.W., Blakesley, R.W., Bouffard, G.G., Beckstrom-Sternberg, S.M., Margulies, E.H., Blanchette, M., Siepel, A.C., Thomas, P.J., McDowell, J.C., Maskeri, B., Hansen,  N.F., Schwartz, M.S., Weber, R.J., Kent, W.J., Karolchik,  D., Bruen, T.C., Bevan, R., Cutler, D.J., Schwartz, S., Elnitski, L., Idol, J.R., Prasad, A.B., Lee-Lin, S.Q., Maduro,  V.V.B., Summers, T.J., Portnoy, M.E., Dietrich, N.L., Akhter, N., Ayele, K., Benjamin, B., Cariaga, K., Brinkley, C.P., Brooks, S.Y., Granite, S., Guan, X., Gupta, J., Haghighi, P., Ho,  S.L., Huang, M.C., Karlins, E., Laric, P.L., Legaspi, R., Lim,  M.J., Maduro, Q.L., Masiello, C.A., Mastrian, S.D., McCloskey,  J.C., Pearson, R., Stantripop, S., Tiongson, E.E., Tran, J.T., Tsurgeon, C., Vogt, J.L., Walker, M.A., Wetherby,  K.D., Wiggins, L.S., Young, A.C., Zhang, L.H., Osoegawa,  K., Zhu, B., Zhao, B., Shu, C.L., Jong, P.J., Lawrence,  C.E., Smit, A.F., Chakravarti, A., Haussler, D., Green,  P., Miller, W., Green, E.D. 2003Comparative analyses of multi-species sequences from targeted genomic regionsNature424788793PubMedCrossRefGoogle Scholar
  37. Uyeno, T., Smith, G.R. 1972Tetraploid origin of the karyotype of catostomid fishesScience175644646PubMedGoogle Scholar
  38. Vasil’ev, V.P. 1999Polyploidization by reticular speciation in acipenseriform evolution: a working hypothesisJ. Appl. Ichthyol.152931CrossRefGoogle Scholar
  39. Venkatesh, B. 2003Evolution and diversity of fish genomesCurr. Opin. Genet. Develop.13588592CrossRefGoogle Scholar
  40. Volff, J.-N. 2005Genome evolution and biodiversity in teleost fishHeredity94280294PubMedCrossRefGoogle Scholar
  41. Wittbrodt, J., Meyer, A., Schartl, M. 1998More genes in fish?Bioessays20511512CrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  1. 1.Department of GeneticsUniversity of GeorgiaAthensUSA
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of CaliforniaIrvineUSA

Personalised recommendations