Boasting nearly 30,000 species, teleosts account for half of all extant vertebrates and approximately 98% of all ray-finned fish species (Actinopterygii). Teleosts are also the largest and most diverse group of vertebrates, exhibiting an astonishing level of morphological, physiological, and behavioral diversity. Previous studies had indicated that the teleost lineage has experienced an additional whole-genome duplication event. Recent comparative genomic analyses of teleosts and other bony vertebrates using spotted gar (a nonteleost ray-finned fish) and elephant shark (a cartilaginous fish) as outgroups have revealed several divergent features of teleost genomes. These include an accelerated evolutionary rate of protein-coding and nucleotide sequences, a higher rate of intron turnover, loss of many potential -regulatory elements and shorter conserved syntenic blocks. A combination of these divergent genomic features might have contributed to the evolution of the amazing phenotypic diversity and morphological innovations of teleosts.


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Literature Cited

  1. 1. Int. Union Conserv. Nat. 2017. The IUCN red list of threatened species, version 2017-2 Cambridge, UK: Int. Union Conserv. Nat. accessed Sep. 14, 2017. http://www.iucnredlist.org. [Google Scholar]
  2. Betancur RR, Broughton RE, Wiley EO, Carpenter K, Lopez JA. 2.  et al. 2013. The tree of life and a new classification of bony fishes. PLOS Curr 5: https://doi.org/10.1371/currents.tol.53ba26640df0ccaee75bb165c8c26288 [Crossref] [Google Scholar]
  3. de Pinna MCC. 3.  1996. Teleostean monophyly. Interrelationships of Fishes MLJ Stiassny, LR Parenti, GD Johnson 147–62 Cambridge, MA: Academic [Google Scholar]
  4. Patterson C, Rosen D. 4.  1977. Review of ichthyodectiform and other Mesozoic teleost fishes and the theory and practice of classifying fossils. Bull. Am. Mus. Nat. Hist. 158:83–172 [Google Scholar]
  5. Near TJ, Eytan RI, Dornburg A, Kuhn KL, Moore JA. 5.  et al. 2012. Resolution of ray-finned fish phylogeny and timing of diversification. PNAS 109:13698–703 [Google Scholar]
  6. Nelson JS, Grande TC, Wilson MVH. 6.  2016. Fishes of the World Hoboken, NJ: Wiley [Google Scholar]
  7. Kocher TD. 7.  2004. Adaptive evolution and explosive speciation: the cichlid fish model. Nat. Rev. Genet. 5:288–98 [Google Scholar]
  8. Wagner CE, Harmon LJ, Seehausen O. 8.  2012. Ecological opportunity and sexual selection together predict adaptive radiation. Nature 487:366–69 [Google Scholar]
  9. Dooley K, Zon LI. 9.  2000. Zebrafish: a model system for the study of human disease. Curr. Opin. Genet. Dev. 10:252–56 [Google Scholar]
  10. Kirchmaier S, Naruse K, Wittbrodt J, Loosli F. 10.  2015. The genomic and genetic toolbox of the teleost medaka (Oryzias latipes). Genetics 199:905–18 [Google Scholar]
  11. Amores A, Force A, Yan YL, Joly L, Amemiya C. 11.  et al. 1998. Zebrafish hox clusters and vertebrate genome evolution. Science 282:1711–14 [Google Scholar]
  12. Christoffels A, Koh EG, Chia JM, Brenner S, Aparicio S, Venkatesh B. 12.  2004. Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes. Mol. Biol. Evol. 21:1146–51 [Google Scholar]
  13. Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N. 13.  et al. 2004. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431:946–57 [Google Scholar]
  14. Taylor JS, Braasch I, Frickey T, Meyer A, Van de Peer Y. 14.  2003. Genome duplication, a trait shared by 22,000 species of ray-finned fish. Genome Res 13:382–90 [Google Scholar]
  15. Aparicio S, Chapman J, Stupka E, Putnam N, Chia JM. 15.  et al. 2002. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. . Science 297:1301–10 [Google Scholar]
  16. Brenner S, Elgar G, Sandford R, Macrae A, Venkatesh B, Aparicio S. 16.  1993. Characterization of the pufferfish (Fugu) genome as a compact model vertebrate genome. Nature 366:265–68 [Google Scholar]
  17. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C. 17.  et al. 2013. The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498–503 [Google Scholar]
  18. Kasahara M, Naruse K, Sasaki S, Nakatani Y, Qu W. 18.  et al. 2007. The medaka draft genome and insights into vertebrate genome evolution. Nature 447:714–19 [Google Scholar]
  19. Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E. 19.  et al. 2012. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:55–61 [Google Scholar]
  20. Venkatesh B, Lee AP, Ravi V, Maurya AK, Lian MM. 20.  et al. 2014. Elephant shark genome provides unique insights into gnathostome evolution. Nature 505:174–79 [Google Scholar]
  21. Braasch I, Gehrke AR, Smith JJ, Kawasaki K, Manousaki T. 21.  et al. 2016. The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons. Nat. Genet. 48:427–37 [Google Scholar]
  22. Amores A, Catchen J, Ferrara A, Fontenot Q, Postlethwait JH. 22.  2011. Genome evolution and meiotic maps by massively parallel DNA sequencing: spotted gar, an outgroup for the teleost genome duplication. Genetics 188:799–808 [Google Scholar]
  23. Lien S, Koop BF, Sandve SR, Miller JR, Kent MP. 23.  et al. 2016. The Atlantic salmon genome provides insights into rediploidization. Nature 533:200–5 [Google Scholar]
  24. Macqueen DJ, Johnston IA. 24.  2014. A well-constrained estimate for the timing of the salmonid whole genome duplication reveals major decoupling from species diversification. Proc. Biol. Sci. 281:20132881 [Google Scholar]
  25. Ohno S, Muramoto J, Christian L, Atkin NB. 25.  1967. Diploid-tetraploid relationship among old-world members of the fish family Cyprinidae. Chromosoma 23:1–9 [Google Scholar]
  26. Xu P, Zhang X, Wang X, Li J, Liu G. 26.  et al. 2014. Genome sequence and genetic diversity of the common carp, Cyprinus carpio. . Nat. Genet. 46:1212–19 [Google Scholar]
  27. Peng Z, Ludwig A, Wang D, Diogo R, Wei Q, He S. 27.  2007. Age and biogeography of major clades in sturgeons and paddlefishes (Pisces: Acipenseriformes). Mol. Phylogenet. Evol. 42:854–62 [Google Scholar]
  28. Lynch M, Conery JS. 28.  2000. The evolutionary fate and consequences of duplicate genes. Science 290:1151–55 [Google Scholar]
  29. Semon M, Wolfe KH. 29.  2007. Reciprocal gene loss between Tetraodon and zebrafish after whole genome duplication in their ancestor. Trends Genet 23:108–12 [Google Scholar]
  30. Taylor JS, Van de Peer Y, Meyer A. 30.  2001. Genome duplication, divergent resolution and speciation. Trends Genet 17:299–301 [Google Scholar]
  31. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. 31.  1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–45 [Google Scholar]
  32. Berthelot C, Brunet F, Chalopin D, Juanchich A, Bernard M. 32.  et al. 2014. The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat. Commun. 5:3657 [Google Scholar]
  33. Clarke JT, Lloyd GT, Friedman M. 33.  2016. Little evidence for enhanced phenotypic evolution in early teleosts relative to their living fossil sister group. PNAS 113:11531–36 [Google Scholar]
  34. Santini F, Harmon LJ, Carnevale G, Alfaro ME. 34.  2009. Did genome duplication drive the origin of teleosts? A comparative study of diversification in ray-finned fishes. BMC Evol. Biol. 9:194 [Google Scholar]
  35. Robertson F, Gundappa MK, Grammes F, Hvidsten T, Redmond A. 35.  et al. 2017. Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification. Genome Biol 18:111 [Google Scholar]
  36. Brawand D, Wagner CE, Li YI, Malinsky M, Keller I. 36.  et al. 2014. The genomic substrate for adaptive radiation in African cichlid fish. Nature 513:375–81 [Google Scholar]
  37. Meier JI, Marques DA, Mwaiko S, Wagner CE, Excoffier L, Seehausen O. 37.  2017. Ancient hybridization fuels rapid cichlid fish adaptive radiations. Nat. Commun. 8:14363 [Google Scholar]
  38. Malmstrom M, Matschiner M, Torresen OK, Star B, Snipen LG. 38.  et al. 2016. Evolution of the immune system influences speciation rates in teleost fishes. Nat. Genet. 48:1204–10 [Google Scholar]
  39. Van de Peer Y, Maere S, Meyer A. 39.  2009. The evolutionary significance of ancient genome duplications. Nat. Rev. Genet. 10:725–32 [Google Scholar]
  40. Fawcett JA, Maere S, Van de Peer Y. 40.  2009. Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. PNAS 106:5737–42 [Google Scholar]
  41. Crow KD, Wagner GP. 41.  2006. Proceedings of the SMBE Tri-National Young Investigators' Workshop 2005: What is the role of genome duplication in the evolution of complexity and diversity?. Mol. Biol. Evol. 23:887–92 [Google Scholar]
  42. Donoghue PC, Purnell MA. 42.  2005. Genome duplication, extinction and vertebrate evolution. Trends Ecol. Evol. 20:312–19 [Google Scholar]
  43. Robinson-Rechavi M, Laudet V. 43.  2001. Evolutionary rates of duplicate genes in fish and mammals. Mol. Biol. Evol. 18:681–83 [Google Scholar]
  44. Britten RJ. 44.  1986. Rates of DNA sequence evolution differ between taxonomic groups. Science 231:1393–98 [Google Scholar]
  45. Martin AP, Palumbi SR. 45.  1993. Body size, metabolic rate, generation time, and the molecular clock. PNAS 90:4087–91 [Google Scholar]
  46. Schlotterer C, Amos B, Tautz D. 46.  1991. Conservation of polymorphic simple sequence loci in cetacean species. Nature 354:63–65 [Google Scholar]
  47. Kottelat M, Britz R, Hui TH, Witte KE. 47.  2006. Paedocypris, a new genus of Southeast Asian cyprinid fish with a remarkable sexual dimorphism, comprises the world's smallest vertebrate. Proc. Biol. Sci. 273:895–99 [Google Scholar]
  48. Pope EC, Hays GC, Thys TM, Doyle TK, Sims DW. 48.  et al. 2010. The biology and ecology of the ocean sunfish Mola: a review of current knowledge and future research perspectives. Rev. Fish Biol. Fish. 20:471–87 [Google Scholar]
  49. Pan H, Yu H, Ravi V, Li C, Lee AP. 49.  et al. 2016. The genome of the largest bony fish, ocean sunfish (Mola mola), provides insights into its fast growth rate. GigaScience 5:36 [Google Scholar]
  50. Richter C, Park JW, Ames BN. 50.  1988. Normal oxidative damage to mitochondrial and nuclear DNA is extensive. PNAS 85:6465–67 [Google Scholar]
  51. Wagner JR, Hu CC, Ames BN. 51.  1992. Endogenous oxidative damage of deoxycytidine in DNA. PNAS 89:3380–84 [Google Scholar]
  52. Seibel BA, Drazen JC. 52.  2007. The rate of metabolism in marine animals: environmental constraints, ecological demands and energetic opportunities. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362:2061–78 [Google Scholar]
  53. Lawrence C, Adatto I, Best J, James A, Maloney K. 53.  2012. Generation time of zebrafish (Danio rerio) and medakas (Oryzias latipes) housed in the same aquaculture facility. Lab. Anim. 41:158–65 [Google Scholar]
  54. Sullivan KJ. 54.  1977. Age and growth of the elephant fish Callorhinchus milii (Elasmobranchii: Callorhynchidae). N. Z. J. Mar. Freshw. Res. 11:745–53 [Google Scholar]
  55. Lynch M, Ackerman MS, Gout JF, Long H, Sung W. 55.  et al. 2016. Genetic drift, selection and the evolution of the mutation rate. Nat. Rev. Genet. 17:704–14 [Google Scholar]
  56. Philip S, Machado JP, Maldonado E, Vasconcelos V, O'Brien SJ. 56.  et al. 2012. Fish lateral line innovation: insights into the evolutionary genomic dynamics of a unique mechanosensory organ. Mol. Biol. Evol. 29:3887–98 [Google Scholar]
  57. Lee AP, Kerk SY, Tan YY, Brenner S, Venkatesh B. 57.  2011. Ancient vertebrate conserved noncoding elements have been evolving rapidly in teleost fishes. Mol. Biol. Evol. 28:1205–15 [Google Scholar]
  58. McLean CY, Reno PL, Pollen AA, Bassan AI, Capellini TD. 58.  et al. 2011. Human-specific loss of regulatory DNA and the evolution of human-specific traits. Nature 471:216–19 [Google Scholar]
  59. Chan YF, Marks ME, Jones FC, Villarreal G Jr., Shapiro MD. 59.  et al. 2010. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327:302–5 [Google Scholar]
  60. Koshikawa S, Giorgianni MW, Vaccaro K, Kassner VA, Yoder JH. 60.  et al. 2015. Gain of cis-regulatory activities underlies novel domains of wingless gene expression in Drosophila. . PNAS 112:7524–29 [Google Scholar]
  61. Wittkopp PJ, Haerum BK, Clark AG. 61.  2008. Regulatory changes underlying expression differences within and between Drosophila species. Nat. Genet. 40:346–50 [Google Scholar]
  62. Coulombe-Huntington J, Majewski J. 62.  2007. Characterization of intron loss events in mammals. Genome Res 17:23–32 [Google Scholar]
  63. Loh YH, Brenner S, Venkatesh B. 63.  2008. Investigation of loss and gain of introns in the compact genomes of pufferfishes (Fugu and Tetraodon). Mol. Biol. Evol. 25:526–35 [Google Scholar]
  64. Roy SW, Fedorov A, Gilbert W. 64.  2003. Large-scale comparison of intron positions in mammalian genes shows intron loss but no gain. PNAS 100:7158–62 [Google Scholar]
  65. Ma MY, Che XR, Porceddu A, Niu DK. 65.  2015. Evaluation of the mechanisms of intron loss and gain in the social amoebae Dictyostelium. . BMC Evol. Biol. 15:286 [Google Scholar]
  66. Roy SW, Gilbert W. 66.  2005. The pattern of intron loss. PNAS 102:713–18 [Google Scholar]
  67. Yenerall P, Krupa B, Zhou L. 67.  2011. Mechanisms of intron gain and loss in Drosophila. . BMC Evol. Biol. 11:364 [Google Scholar]
  68. Farlow A, Meduri E, Schlotterer C. 68.  2011. DNA double-strand break repair and the evolution of intron density. Trends Genet 27:1–6 [Google Scholar]
  69. Fawcett JA, Rouze P, Van de Peer Y. 69.  2012. Higher intron loss rate in Arabidopsis thaliana than A. lyrata is consistent with stronger selection for a smaller genome. Mol. Biol. Evol. 29:849–59 [Google Scholar]
  70. Yenerall P, Zhou L. 70.  2012. Identifying the mechanisms of intron gain: progress and trends. Biol. Direct 7:29 [Google Scholar]
  71. Roy SW, Irimia M. 71.  2009. Mystery of intron gain: new data and new models. Trends Genet 25:67–73 [Google Scholar]
  72. Torriani SF, Stukenbrock EH, Brunner PC, McDonald BA, Croll D. 72.  2011. Evidence for extensive recent intron transposition in closely related fungi. Curr. Biol. 21:2017–22 [Google Scholar]
  73. Denoeud F, Henriet S, Mungpakdee S, Aury JM, Da Silva C. 73.  et al. 2010. Plasticity of animal genome architecture unmasked by rapid evolution of a pelagic tunicate. Science 330:1381–85 [Google Scholar]
  74. Huff JT, Zilberman D, Roy SW. 74.  2016. Mechanism for DNA transposons to generate introns on genomic scales. Nature 538:533–36 [Google Scholar]
  75. Gao X, Lynch M. 75.  2009. Ubiquitous internal gene duplication and intron creation in eukaryotes. PNAS 106:20818–23 [Google Scholar]
  76. Sharpton TJ, Neafsey DE, Galagan JE, Taylor JW. 76.  2008. Mechanisms of intron gain and loss in Cryptococcus. . Genome Biol 9:R24 [Google Scholar]
  77. Zhang LY, Yang YF, Niu DK. 77.  2010. Evaluation of models of the mechanisms underlying intron loss and gain in Aspergillus fungi. J. Mol. Evol. 71:364–73 [Google Scholar]
  78. Li W, Tucker AE, Sung W, Thomas WK, Lynch M. 78.  2009. Extensive, recent intron gains in Daphnia populations. Science 326:1260–62 [Google Scholar]
  79. Chalopin D, Naville M, Plard F, Galiana D, Volff JN. 79.  2015. Comparative analysis of transposable elements highlights mobilome diversity and evolution in vertebrates. Genome Biol. Evol. 7:567–80 [Google Scholar]
  80. Burns KH, Boeke JD. 80.  2012. Human transposon tectonics. Cell 149:740–52 [Google Scholar]
  81. Kazazian HH Jr.. 81.  2004. Mobile elements: drivers of genome evolution. Science 303:1626–32 [Google Scholar]
  82. Castillo-Davis CI, Bedford TB, Hartl DL. 82.  2004. Accelerated rates of intron gain/loss and protein evolution in duplicate genes in human and mouse malaria parasites. Mol. Biol. Evol. 21:1422–27 [Google Scholar]
  83. Juneau K, Miranda M, Hillenmeyer ME, Nislow C, Davis RW. 83.  2006. Introns regulate RNA and protein abundance in yeast. Genetics 174:511–18 [Google Scholar]
  84. Shabalina SA, Ogurtsov AY, Spiridonov AN, Novichkov PS, Spiridonov NA, Koonin EV. 84.  2010. Distinct patterns of expression and evolution of intronless and intron-containing mammalian genes. Mol. Biol. Evol. 27:1745–49 [Google Scholar]
  85. Bejerano G, Pheasant M, Makunin I, Stephen S, Kent WJ. 85.  et al. 2004. Ultraconserved elements in the human genome. Science 304:1321–25 [Google Scholar]
  86. Lindblad-Toh K, Garber M, Zuk O, Lin MF, Parker BJ. 86.  et al. 2011. A high-resolution map of human evolutionary constraint using 29 mammals. Nature 478:476–82 [Google Scholar]
  87. Shin JT, Priest JR, Ovcharenko I, Ronco A, Moore RK. 87.  et al. 2005. Human-zebrafish non-coding conserved elements act in vivo to regulate transcription. Nucleic Acids Res 33:5437–45 [Google Scholar]
  88. Woolfe A, Goodson M, Goode DK, Snell P, McEwen GK. 88.  et al. 2005. Highly conserved non-coding sequences are associated with vertebrate development. PLOS Biol 3:e7 [Google Scholar]
  89. Sandelin A, Bailey P, Bruce S, Engstrom PG, Klos JM. 89.  et al. 2004. Arrays of ultraconserved non-coding regions span the loci of key developmental genes in vertebrate genomes. BMC Genom 5:99 [Google Scholar]
  90. Navratilova P, Fredman D, Hawkins TA, Turner K, Lenhard B, Becker TS. 90.  2009. Systematic human/zebrafish comparative identification of cis-regulatory activity around vertebrate developmental transcription factor genes. Dev. Biol. 327:526–40 [Google Scholar]
  91. Visel A, Prabhakar S, Akiyama JA, Shoukry M, Lewis KD. 91.  et al. 2008. Ultraconservation identifies a small subset of extremely constrained developmental enhancers. Nat. Genet. 40:158–60 [Google Scholar]
  92. Aparicio S, Morrison A, Gould A, Gilthorpe J, Chaudhuri C. 92.  et al. 1995. Detecting conserved regulatory elements with the model genome of the Japanese puffer fish, Fugu rubripes. . PNAS 92:1684–88 [Google Scholar]
  93. Pennacchio LA, Ahituv N, Moses AM, Prabhakar S, Nobrega MA. 93.  et al. 2006. In vivo enhancer analysis of human conserved non-coding sequences. Nature 444:499–502 [Google Scholar]
  94. Venkatesh B, Kirkness EF, Loh YH, Halpern AL, Lee AP. 94.  et al. 2006. Ancient noncoding elements conserved in the human genome. Science 314:1892 [Google Scholar]
  95. Carroll SB. 95.  2008. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134:25–36 [Google Scholar]
  96. Wray GA. 96.  2007. The evolutionary significance of cis-regulatory mutations. Nat. Rev. Genet. 8:206–16 [Google Scholar]
  97. Indjeian VB, Kingman GA, Jones FC, Guenther CA, Grimwood J. 97.  et al. 2016. Evolving new skeletal traits by cis-regulatory changes in bone morphogenetic proteins. Cell 164:45–56 [Google Scholar]
  98. Attanasio C, Nord AS, Zhu Y, Blow MJ, Li Z. 98.  et al. 2013. Fine tuning of craniofacial morphology by distant-acting enhancers. Science 342:1241006 [Google Scholar]
  99. Ravi V, Bhatia S, Gautier P, Loosli F, Tay BH. 99.  et al. 2013. Sequencing of Pax6 loci from the elephant shark reveals a family of Pax6 genes in vertebrate genomes, forged by ancient duplications and divergences. PLOS Genet 9:e1003177 [Google Scholar]
  100. Kikuta H, Laplante M, Navratilova P, Komisarczuk AZ, Engstrom PG. 100.  et al. 2007. Genomic regulatory blocks encompass multiple neighboring genes and maintain conserved synteny in vertebrates. Genome Res 17:545–55 [Google Scholar]
  101. Lee AP, Koh EG, Tay A, Brenner S, Venkatesh B. 101.  2006. Highly conserved syntenic blocks at the vertebrate Hox loci and conserved regulatory elements within and outside Hox gene clusters. PNAS 103:6994–99 [Google Scholar]
  102. Maeso I, Irimia M, Tena JJ, Gonzalez-Perez E, Tran D. 102.  et al. 2012. An ancient genomic regulatory block conserved across bilaterians and its dismantling in tetrapods by retrogene replacement. Genome Res 22:642–55 [Google Scholar]
  103. Lee JH, Silhavy JL, Lee JE, Al-Gazali L, Thomas S. 103.  et al. 2012. Evolutionarily assembled cis-regulatory module at a human ciliopathy locus. Science 335:966–69 [Google Scholar]
  104. Venkatesh B, Ravi V, Lee AP, Warren WC, Brenner S. 104.  2013. Basal vertebrates clarify the evolutionary history of ciliopathy-associated genes Tmem138 and Tmem216. . Mol. Biol. Evol. 30:62–65 [Google Scholar]
  105. Bian C, Hu Y, Ravi V, Kuznetsova IS, Shen X. 105.  et al. 2016. The Asian arowana (Scleropages formosus) genome provides new insights into the evolution of an early lineage of teleosts. Sci. Rep. 6:24501 [Google Scholar]

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