Hydrobiologia

, Volume 625, Issue 1, pp 1–25 | Cite as

Patterns of genome size diversity in the ray-finned fishes

Review Article

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.

Keywords

Actinopterygii Climate Morphology Physiology Polyploidy Teleosts 

References

  1. Abrusán, G. & H.-J. Krambeck, 2006. Competition may determine the diversity of transposable elements. Theoretical Population Biology 70: 364–375.PubMedCrossRefGoogle Scholar
  2. Andrews, C. B. & T. R. Gregory, 2009. Genome size is inversely correlated with relative brain size in parrots and cockatoos. Genome (in press).Google Scholar
  3. 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.PubMedCrossRefGoogle Scholar
  4. Arkhipchuk, V. V., 1995. Role of chromosomal and genome mutations in the evolution of bony fishes. Hydrobiological Journal 31: 55–65.Google Scholar
  5. 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
  6. Bennett, M. D., 1976. DNA amount, latitude, and crop plant distribution. Environmental and Experimental Botany 16: 93–108.CrossRefGoogle Scholar
  7. Bennett, M. D., 1987. Variation in genomic form in plants and its ecological implications. New Phytologist 106(Suppl): 177–200.Google Scholar
  8. 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.PubMedGoogle Scholar
  9. Brookfield, J. F. Y., 2005. The ecology of the genome—mobile DNA elements and their hosts. Nature Reviews Genetics 6: 128–136.PubMedCrossRefGoogle Scholar
  10. 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
  11. Charlesworth, B. & N. Barton, 2004. Genome size: does bigger mean worse? Current Biology 14: R233–R235.PubMedCrossRefGoogle Scholar
  12. 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.CrossRefGoogle Scholar
  13. 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
  14. 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.CrossRefGoogle Scholar
  15. Froese, R. & D. Pauly, 2008. FishBase [available on the internet at http://www.fishbase.org].
  16. 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.Google Scholar
  17. Gregory, T. R., 2001a. Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biological Reviews 76: 65–101.PubMedCrossRefGoogle Scholar
  18. 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.PubMedCrossRefGoogle Scholar
  19. 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.PubMedGoogle Scholar
  20. Gregory, T. R., 2002b. Genome size and developmental parameters in the homeothermic vertebrates. Genome 45: 833–838.PubMedCrossRefGoogle Scholar
  21. Gregory, T. R., 2002c. Genome size and developmental complexity. Genetica 115: 131–146.PubMedCrossRefGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. Gregory, T. R., 2004a. Genome size is not positively correlated with longevity in fishes (or homeotherms). Experimental Gerontology 39: 859–860.CrossRefGoogle Scholar
  24. Gregory, T. R., 2004b. Insertion–deletion biases and the evolution of genome size. Gene 324: 15–34.PubMedCrossRefGoogle Scholar
  25. 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
  26. Gregory, T. R., 2005b. Synergy between sequence and size in large-scale genomics. Nature Reviews Genetics 6: 699–708.PubMedCrossRefGoogle Scholar
  27. Gregory, T. R., 2008. Animal Genome Size Database [available on the internet at http://www.genomesize.com].
  28. 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
  29. Gregory, T. R. & J. D. S. Witt, 2008. Population size and genome size in fishes: a closer look. Genome 51: 309–313.PubMedCrossRefGoogle Scholar
  30. 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.PubMedCrossRefGoogle Scholar
  31. 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.CrossRefGoogle Scholar
  32. Griffith, O. L., G. E. E. Moodie & A. Civetta, 2003. Genome size and longevity in fish. Experimental Gerontology 38: 333–337.PubMedCrossRefGoogle Scholar
  33. 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.PubMedCrossRefGoogle Scholar
  34. Hardie, D. C. & P. D. N. Hebert, 2004. Genome-size evolution in fishes. Canadian Journal of Fisheries and Aquatic Sciences 61: 1636–1646.CrossRefGoogle Scholar
  35. 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.PubMedGoogle Scholar
  36. Hinegardner, R., 1968. Evolution of cellular DNA content in teleost fishes. American Naturalist 102: 517–523.CrossRefGoogle Scholar
  37. Hinegardner, R., 1976. Evolution of genome size. In Ayala, F. J. (ed.), Molecular Evolution. Sinauer Associates, Inc, Sunderland: 179–199.Google Scholar
  38. Hinegardner, R. & D. E. Rosen, 1972. Cellular DNA content and the evolution of teleostean fishes. American Naturalist 106: 621–644.CrossRefGoogle Scholar
  39. International Chicken Genome Sequencing Consortium, 2004. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432: 695–777.CrossRefGoogle Scholar
  40. International Human Genome Sequencing Consortium, 2001. Initial sequencing and analysis of the human genome. Nature 409: 860–921.CrossRefGoogle Scholar
  41. 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.PubMedCrossRefGoogle Scholar
  42. John, B. & G. L. G. Miklos, 1988. The Eukaryote Genome in Development and Evolution. Allen & Unwin, London.Google Scholar
  43. 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.PubMedCrossRefGoogle Scholar
  44. Kidwell, M. G., 2002. Transposable elements and the evolution of genome size in eukaryotes. Genetica 115: 49–63.PubMedCrossRefGoogle Scholar
  45. 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/].
  46. Lynch, M. & J. S. Conery, 2003. The origins of genome complexity. Science 302: 1401–1404.PubMedCrossRefGoogle Scholar
  47. 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.CrossRefGoogle Scholar
  48. Mank, J. E. & J. C. Avise, 2006b. Phylogenetic conservation of chromosome numbers in Actinopterygiian fishes. Genetica 127: 321–327.PubMedCrossRefGoogle Scholar
  49. 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.PubMedGoogle Scholar
  50. Mirsky, A. E. & H. Ris, 1951. The desoxyribonucleic acid content of animal cells and its evolutionary significance. Journal of General Physiology 34: 451–462.PubMedCrossRefGoogle Scholar
  51. Monaghan, P. & N. B. Metcalfe, 2000. Genome size and longevity. Trends in Genetics 16: 331–332.PubMedCrossRefGoogle Scholar
  52. Monaghan, P. & N. B. Metcalfe, 2001. Genome size, longevity and development time in birds. Trends in Genetics 17: 568.CrossRefGoogle Scholar
  53. Morand, S. & R. E. Ricklefs, 2001. Genome size, longevity and development time in birds. Trends in Genetics 17: 567–568.PubMedCrossRefGoogle Scholar
  54. Morand, S. & R. E. Ricklefs, 2005. Genome size is not related to life-history traits in primates. Genome 48: 273–278.PubMedGoogle Scholar
  55. 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.PubMedCrossRefGoogle Scholar
  56. Ohno, S., 1974. Animal Cytogenetics, Vol. 4. Chordata 1: Protochordata, Cyclostomata, and Pisces. Gebrüder Borntraeger, Berlin.Google Scholar
  57. 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.PubMedCrossRefGoogle Scholar
  58. Olmo, E., 2006. Genome size and evolutionary diversification in vertebrates. Italian Journal of Zoology 73: 167–171.CrossRefGoogle Scholar
  59. Petrov, D. A., 2002. Mutational equilibrium model of genome size evolution. Theoretical Population Biology 61: 533–546.CrossRefGoogle Scholar
  60. 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.PubMedCrossRefGoogle Scholar
  61. 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.Google Scholar
  62. 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.Google Scholar
  63. Venkatesh, B., 2003. Evolution and diversity of fish genomes. Current Opinion in Genetics & Development 13: 588–592.CrossRefGoogle Scholar
  64. 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.CrossRefGoogle Scholar
  65. Vinogradov, A. E., 2003. Selfish DNA is maladaptive: evidence from the plant Red List. Trends in Genetics 19: 609–614.PubMedCrossRefGoogle Scholar
  66. Vinogradov, A. E., 2004a. Genome size and extinction risk in vertebrates. Proceedings of the Royal Society of London B 271: 1701–1705.CrossRefGoogle Scholar
  67. Vinogradov, A. E., 2004b. Testing genome complexity. Science 304: 389–390.PubMedCrossRefGoogle Scholar
  68. Yi, S. V., 2006. Non-adaptive evolution of genome complexity. BioEssays 28: 979–982.PubMedCrossRefGoogle Scholar
  69. 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.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Department of Integrative BiologyUniversity of GuelphGuelphCanada
  2. 2.Department of BiologyMcMaster UniversityHamiltonCanada

Personalised recommendations