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Patterns of genome size diversity in the ray-finned fishes

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Abstract

The ray-finned fishes make up about half of all vertebrate diversity and are by far the best represented group in the Animal Genome Size Database. However, they have traditionally been the least well investigated among vertebrates in terms of patterns and consequences of genome size diversity. This article synthesizes and expands upon existing information about genome size diversity in ray-finned fishes. Specifically, compiled data from the Animal Genome Size Database and FishBase are used to examine the potential patterns of interspecific genome size variability according to ecology, environment, morphology, growth, physiology, reproduction, longevity, and taxonomic diversity. Polyploidy and haploid genome sizes are considered separately, revealing differences in their respective consequences. This represents the most comprehensive summary of fish genome size diversity presented to date, and highlights areas of particular interest to investigate as more data become available.

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References

  • Abrusán, G. & H.-J. Krambeck, 2006. Competition may determine the diversity of transposable elements. Theoretical Population Biology 70: 364–375.

    Article  PubMed  Google Scholar 

  • Andrews, C. B. & T. R. Gregory, 2009. Genome size is inversely correlated with relative brain size in parrots and cockatoos. Genome (in press).

  • Aparicio, S., J. Chapman, E. Stupka, N. Putnam, J.-m. Chia, P. Dehal, A. Christoffels, S. Rash, S. Hoon, A. Smit, M. D. Sollewjin Gelpke, J. Roach, T. Oh, I. Y. Ho, M. Wong, C. Detter, F. Verhoef, P. Predki, A. Tay, S. Lucas, P. Richardson, S. F. Smith, M. S. Clark, Y. J. K. Edwards, N. Doggett, A. Zharkik, S. V. Tavtigian, D. Pruss, M. Barnstead, C. Evans, H. Baden, J. Powell, G. Glusman, L. Rowen, L. Hood, Y. H. Tan, G. Elgar, T. Hawkins, B. Venkatesh, D. Rokhsar & S. Brenner, 2002. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297: 1301–1310.

    Article  PubMed  CAS  Google Scholar 

  • Arkhipchuk, V. V., 1995. Role of chromosomal and genome mutations in the evolution of bony fishes. Hydrobiological Journal 31: 55–65.

    Google Scholar 

  • Balon, E. K., 1990. Epigenesis of an epigeneticist: the development of some alternative concepts on the early ontogeny and evolution of fishes. Guelph Ichthyology Reviews 1: 1–48.

    Google Scholar 

  • Bennett, M. D., 1976. DNA amount, latitude, and crop plant distribution. Environmental and Experimental Botany 16: 93–108.

    Article  CAS  Google Scholar 

  • Bennett, M. D., 1987. Variation in genomic form in plants and its ecological implications. New Phytologist 106(Suppl): 177–200.

    Google Scholar 

  • Brainerd, E. L., S. S. Slutz, E. K. Hall & R. W. Phillis, 2001. Patterns of genome size evolution in tetraodontiform fishes. Evolution 55: 2363–2368.

    PubMed  CAS  Google Scholar 

  • Brookfield, J. F. Y., 2005. The ecology of the genome—mobile DNA elements and their hosts. Nature Reviews Genetics 6: 128–136.

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith, T., 1985. Introduction: the evolutionary significance of genome size. In Cavalier-Smith, T. (ed.), The Evolution of Genome Size. Wiley, Chichester, UK: 1–36.

    Google Scholar 

  • Charlesworth, B. & N. Barton, 2004. Genome size: does bigger mean worse? Current Biology 14: R233–R235.

    Article  PubMed  CAS  Google Scholar 

  • Civetta, A., O. L. Griffith & G. E. E. Moodie, 2004. Reply to Gregory’s letter to the editor: genome size and its correlation with longevity in fishes. Experimental Gerontology 39: 861–862.

    Article  CAS  Google Scholar 

  • Costantini, D., L. Racheli, D. Cavallo & G. Dell’Omo, 2008. Genome size variation in parrots: longevity and flying ability. Journal of Avian Biology 39: 453–459.

    Google Scholar 

  • Ebeling, A. W., N. B. Atkin & P. Y. Setzer, 1971. Genome sizes of teleostean fishes: increases in some deep-sea species. American Naturalist 105: 549–561.

    Article  Google Scholar 

  • Froese, R. & D. Pauly, 2008. FishBase [available on the internet at http://www.fishbase.org].

  • Graham, M. S., R. L. Haedrich & G. L. Fletcher, 1985. Hematology of three deep-sea fishes: a reflection of low metabolic rates. Comparative Biochemistry and Physiology 80A: 79–84.

    CAS  Google Scholar 

  • Gregory, T. R., 2001a. Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biological Reviews 76: 65–101.

    Article  PubMed  CAS  Google Scholar 

  • Gregory, T. R., 2001b. The bigger the C-value, the larger the cell: genome size and red blood cell size in vertebrates. Blood Cells, Molecules, and Diseases 27: 830–843.

    Article  PubMed  CAS  Google Scholar 

  • Gregory, T. R., 2002a. A bird’s-eye view of the C-value enigma: genome size, cell size, and metabolic rate in the class Aves. Evolution 56: 121–130.

    PubMed  CAS  Google Scholar 

  • Gregory, T. R., 2002b. Genome size and developmental parameters in the homeothermic vertebrates. Genome 45: 833–838.

    Article  PubMed  CAS  Google Scholar 

  • Gregory, T. R., 2002c. Genome size and developmental complexity. Genetica 115: 131–146.

    Article  PubMed  Google Scholar 

  • Gregory, T. R., 2003. Variation across amphibian species in the size of the nuclear genome supports a pluralistic, hierarchical approach to the C-value enigma. Biological Journal of the Linnean Society 79: 329–339.

    Article  Google Scholar 

  • Gregory, T. R., 2004a. Genome size is not positively correlated with longevity in fishes (or homeotherms). Experimental Gerontology 39: 859–860.

    Article  CAS  Google Scholar 

  • Gregory, T. R., 2004b. Insertion–deletion biases and the evolution of genome size. Gene 324: 15–34.

    Article  PubMed  CAS  Google Scholar 

  • Gregory, T. R., 2005a. Genome size evolution in animals. In Gregory, T. R. (ed.), The Evolution of the Genome. Elsevier, San Diego: 3–87.

    Google Scholar 

  • Gregory, T. R., 2005b. Synergy between sequence and size in large-scale genomics. Nature Reviews Genetics 6: 699–708.

    Article  PubMed  CAS  Google Scholar 

  • Gregory, T. R., 2008. Animal Genome Size Database [available on the internet at http://www.genomesize.com].

  • Gregory, T. R. & B. K. Mable, 2005. Polyploidy in animals. In Gregory, T. R. (ed.), The Evolution of the Genome. Elsevier, San Diego: 427–517.

    Google Scholar 

  • Gregory, T. R. & J. D. S. Witt, 2008. Population size and genome size in fishes: a closer look. Genome 51: 309–313.

    Article  PubMed  Google Scholar 

  • Gregory, T. R., P. D. N. Hebert & J. Kolasa, 2000. Evolutionary implications of the relationship between genome size and body size in flatworms and copepods. Heredity 84: 201–208.

    Article  PubMed  Google Scholar 

  • Gregory, T. R., J. A. Nicol, H. Tamm, B. Kullman, K. Kullman, I. J. Leitch, B. G. Murray, D. F. Kapraun, J. Greilhuber & M. D. Bennett, 2007. Eukaryotic genome size databases. Nucleic Acids Research 35(Database Issue): 332–338.

    Article  Google Scholar 

  • Griffith, O. L., G. E. E. Moodie & A. Civetta, 2003. Genome size and longevity in fish. Experimental Gerontology 38: 333–337.

    Article  PubMed  CAS  Google Scholar 

  • Hardie, D. C. & P. D. N. Hebert, 2003. The nucleotypic effects of cellular DNA content in cartilaginous and ray-finned fishes. Genome 46: 683–706.

    Article  PubMed  CAS  Google Scholar 

  • Hardie, D. C. & P. D. N. Hebert, 2004. Genome-size evolution in fishes. Canadian Journal of Fisheries and Aquatic Sciences 61: 1636–1646.

    Article  Google Scholar 

  • Hardie, D. C., T. R. Gregory & P. D. N. Hebert, 2002. From pixels to picograms: a beginners’ guide to genome quantification by Feulgen image analysis densitometry. Journal of Histochemistry and Cytochemistry 50: 735–749.

    PubMed  CAS  Google Scholar 

  • Hinegardner, R., 1968. Evolution of cellular DNA content in teleost fishes. American Naturalist 102: 517–523.

    Article  Google Scholar 

  • Hinegardner, R., 1976. Evolution of genome size. In Ayala, F. J. (ed.), Molecular Evolution. Sinauer Associates, Inc, Sunderland: 179–199.

    Google Scholar 

  • Hinegardner, R. & D. E. Rosen, 1972. Cellular DNA content and the evolution of teleostean fishes. American Naturalist 106: 621–644.

    Article  CAS  Google Scholar 

  • International Chicken Genome Sequencing Consortium, 2004. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432: 695–777.

    Article  Google Scholar 

  • International Human Genome Sequencing Consortium, 2001. Initial sequencing and analysis of the human genome. Nature 409: 860–921.

    Article  Google Scholar 

  • Jaillon, O., J. M. Aury, F. Brunet, J. L. Petit, N. Stange-Thomann, E. Mauceli, L. Bouneau, C. Fischer, C. Ozouf-Costaz, A. Bernot, S. Nicaud, D. Jaffe, S. Fisher, G. Lutfalla, C. Dossat, B. Segurens, C. Dasilva, M. Salanoubat, M. Levy, N. Boudet, S. Castellano, V. Anthouard, C. Jubin, V. Castelli, M. Katinka, B. Vacherie, C. Biémont, Z. Skalli, L. Cattolico, J. Poulain, V. De Berardinis, C. Cruaud, S. Duprat, P. Brottier, J. P. Coutanceau, J. Gouzy, G. Parra, G. Lardier, C. Chapple, K. J. McKernan, P. McEwan, S. Bosak, M. Kellis, J. N. Volff, R. Guigó, M. C. Zody, J. Mesirov, K. Lindblad-Toh, B. Birren, C. Nusbaum, D. Kahn, M. Robinson-Rechavi, V. Laudet, V. Schachter, F. Quétier, W. Saurin, C. Scarpelli, P. Wincker, E. S. Lander, J. Weissenbach & H. Roest Crollius, 2004. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431: 946–957.

    Article  PubMed  Google Scholar 

  • John, B. & G. L. G. Miklos, 1988. The Eukaryote Genome in Development and Evolution. Allen & Unwin, London.

    Google Scholar 

  • Kasahara, M., K. Naruse, S. Sasaki, Y. Nakatani, W. Qu, B. Ahsan, T. Yamada, Y. Nagayasu, K. Doi, Y. Kasai, T. Jindo, D. Kobayashi, A. Shimada, A. Toyoda, Y. Kuroki, A. Fujiyama, T. Sasaki, A. Shimizu, S. Asakawa, N. Shimizu, S.-i. Hashimoto, J. Yang, Y. Lee, K. Matsushima, S. Sugano, M. Sakaizumi, T. Narita, K. Ohishi, S. Haga, F. Ohta, H. Nomoto, K. Nogata, T. Morishita, T. Endo, T. Shin-I, H. Takeda, S. Morishita & Y. Kohara, 2007. The medaka draft genome and insights into vertebrate genome evolution. Nature 447: 714–719.

    Article  PubMed  CAS  Google Scholar 

  • Kidwell, M. G., 2002. Transposable elements and the evolution of genome size in eukaryotes. Genetica 115: 49–63.

    Article  PubMed  CAS  Google Scholar 

  • Liolios, K., K. Mavrommatis, N. Tavernarakis & N. C. Kyrpides, 2008. The Genomes on Line Database (GOLD) in 2007: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Research 36 (Database Issue): D475–D479 [available on internet at http://www.genomesonline.org/].

  • Lynch, M. & J. S. Conery, 2003. The origins of genome complexity. Science 302: 1401–1404.

    Article  PubMed  CAS  Google Scholar 

  • Mank, J. E. & J. C. Avise, 2006a. Cladogenetic correlates of genomic expansions in the recent evolution of actinopterygiian fishes. Proceedings of the Royal Society of London B 273: 33–38.

    Article  Google Scholar 

  • Mank, J. E. & J. C. Avise, 2006b. Phylogenetic conservation of chromosome numbers in Actinopterygiian fishes. Genetica 127: 321–327.

    Article  PubMed  Google Scholar 

  • Mank, J. E., D. E. L. Promislow & J. C. Avise, 2005. Phylogenetic perspectives in the evolution of parental care in ray-finned fishes. Evolution 59: 1570–1578.

    PubMed  Google Scholar 

  • Mirsky, A. E. & H. Ris, 1951. The desoxyribonucleic acid content of animal cells and its evolutionary significance. Journal of General Physiology 34: 451–462.

    Article  PubMed  CAS  Google Scholar 

  • Monaghan, P. & N. B. Metcalfe, 2000. Genome size and longevity. Trends in Genetics 16: 331–332.

    Article  PubMed  CAS  Google Scholar 

  • Monaghan, P. & N. B. Metcalfe, 2001. Genome size, longevity and development time in birds. Trends in Genetics 17: 568.

    Article  CAS  Google Scholar 

  • Morand, S. & R. E. Ricklefs, 2001. Genome size, longevity and development time in birds. Trends in Genetics 17: 567–568.

    Article  PubMed  CAS  Google Scholar 

  • Morand, S. & R. E. Ricklefs, 2005. Genome size is not related to life-history traits in primates. Genome 48: 273–278.

    PubMed  CAS  Google Scholar 

  • Neafsey, D. E. & S. R. Palumbi, 2003. Genome size evolution in pufferfish: a comparative analysis of diodontid and tetraodontid pufferfish genomes. Genome Research 13: 821–830.

    Article  PubMed  CAS  Google Scholar 

  • Ohno, S., 1974. Animal Cytogenetics, Vol. 4. Chordata 1: Protochordata, Cyclostomata, and Pisces. Gebrüder Borntraeger, Berlin.

  • Olmo, E., 2003. Reptiles: a group of transition in the evolution of genome size and of the nucleotypic effect. Cytogenetic and Genome Research 101: 166–171.

    Article  PubMed  CAS  Google Scholar 

  • Olmo, E., 2006. Genome size and evolutionary diversification in vertebrates. Italian Journal of Zoology 73: 167–171.

    Article  CAS  Google Scholar 

  • Petrov, D. A., 2002. Mutational equilibrium model of genome size evolution. Theoretical Population Biology 61: 533–546.

    Article  Google Scholar 

  • Rees, D. J., F. Dufresne, H. Glémet & C. Belzile, 2007. Amphipod genome sizes: first estimates for Arctic species reveal genomic giants. Genome 50: 151–158.

    Article  PubMed  CAS  Google Scholar 

  • Vendrely, R. & C. Vendrely, 1950. Sur la teneur absolue en acide désoxyribonucléique du noyau cellulaire chez quelques espèces d’oiseaux et de poissons. Comptes Rendus de l’Académie des Sciences 230: 788–790.

    CAS  Google Scholar 

  • Vendrely, R. & C. Vendrely, 1952. Sur la teneur comparée en arginine et en acide désoxyribonucléique des noyaux d’érythrocytes de quelques espèces de poissons. Comptes Rendus de l’Académie des Sciences 235: 395–397.

    CAS  Google Scholar 

  • Venkatesh, B., 2003. Evolution and diversity of fish genomes. Current Opinion in Genetics & Development 13: 588–592.

    Article  CAS  Google Scholar 

  • Vinogradov, A. E., 1995. Nucleotypic effect in homeotherms: body mass-corrected basal metabolic rate of mammals is related to genome size. Evolution 49: 1249–1259.

    Article  Google Scholar 

  • Vinogradov, A. E., 2003. Selfish DNA is maladaptive: evidence from the plant Red List. Trends in Genetics 19: 609–614.

    Article  PubMed  CAS  Google Scholar 

  • Vinogradov, A. E., 2004a. Genome size and extinction risk in vertebrates. Proceedings of the Royal Society of London B 271: 1701–1705.

    Article  Google Scholar 

  • Vinogradov, A. E., 2004b. Testing genome complexity. Science 304: 389–390.

    Article  PubMed  CAS  Google Scholar 

  • Yi, S. V., 2006. Non-adaptive evolution of genome complexity. BioEssays 28: 979–982.

    Article  PubMed  CAS  Google Scholar 

  • Yi, S. & J. T. Streelman, 2005. Genome size is negatively correlated with effective population size in ray-finned fishes. Trends in Genetics 21: 643–646.

    Article  PubMed  CAS  Google Scholar 

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  1. Emily M. Smith

    Present address: Department of Biology, McMaster University, Hamilton, ON, L8S 4K1, Canada

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  1. Department of Integrative Biology, University of Guelph, Guelph, ON, N1G 2W1, Canada

    Emily M. Smith & T. Ryan Gregory

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Handling editor: Christian Straumber

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Smith, E.M., Gregory, T.R. Patterns of genome size diversity in the ray-finned fishes. Hydrobiologia 625, 1–25 (2009). https://doi.org/10.1007/s10750-009-9724-x

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