Abstract
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.
Similar content being viewed by others
References
F.W. Allendorf G.H. Thorgaard (1984) Tetraploidy and the evolution of Salmonid fishes B.J. Turner (Eds) Evolutionary Genetics of Fishes Plenum Press New York 1–53
A. Amores T. Suzuki Y.L. Yan J. Pomeroy A. Singer C. Amemiya J.H. Postlethwait (2004) ArticleTitleDevelopmental roles of pufferfish Hox clusters and genome evolution in ray-finned fish Genome Res. 14 1–10 Occurrence Handle14707165 Occurrence Handle1:CAS:528:DC%2BD2cXlvVGntg%3D%3D Occurrence Handle10.1101/gr.1717804
S. Aparicio J. Chapman E. Stupka N. Putnam J. Chia P. Dehal A. Christoffels S. Rash S. Hoon A. Smit M.D.S. 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. Zharkikh 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) ArticleTitleWhole-genome shotgun assembly and analysis of the genome of Fugu rubripes Science 297 1301–1310 Occurrence Handle12142439 Occurrence Handle1:CAS:528:DC%2BD38Xms1ejtr8%3D Occurrence Handle10.1126/science.1072104
V.V. Arkhipchuk (1995) ArticleTitleRole of chromosomal and genome mutations in the evolution of bony fishes Hydrobiologia 31 55–65
S.P. Blomberg T. Garland (2002) ArticleTitleTempo and mode in evolution: phylogenetic inertia, adaptation, and comparative methods J. Evolution. Biol. 15 899–910 Occurrence Handle10.1046/j.1420-9101.2002.00472.x
A. Christoffels E.G.L. Koh J.-M. Chia S. Brenner S. Aparicio B. Venkatesh (2004) ArticleTitleFugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes Mol. Biol. Evolution 21 1146–1151 Occurrence Handle1:CAS:528:DC%2BD2cXksVymu7s%3D Occurrence Handle10.1093/molbev/msh114
L.F. Almeida-Toledo Particlede M.F.Z. Daniel-Silva C.B. Moyses S.B.A. Fonteles C.E. Lopes A. Akama F. Foresti (2002) ArticleTitleChromosome evolution in a fish: sex chromosome variability in Eigenmannia virescens (Gymnotiformes: Sternopygidae) Cytogen. Genome Res. 99 164–169 Occurrence Handle10.1159/000071589
R.H. Devlin Y. Nagahama (2002) ArticleTitleSex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences Aquaculture 208 191–364 Occurrence Handle1:CAS:528:DC%2BD38XktFKjsbY%3D Occurrence Handle10.1016/S0044-8486(02)00057-1
S.D. Ferris (1984) Tetraploidy and the evolution of catostomid fishes B.J. Turner (Eds) Evolutionary Genetics of Fish Plenum Press New York
A. Force M. Lynch F.B. Pickett A. Amores Y.L. Yan J. Postlethwait (1999) ArticleTitlePreservation of duplicate genes by complementary, degenerative mutations Genetics 151 1531–1545 Occurrence Handle10101175 Occurrence Handle1:CAS:528:DyaK1MXisV2rs7o%3D
Gregory, T.R., 2005. Animal Genome Size Database. http://www.genomesize.com
R. Hinegardner (1976) Evolution of genome size F.J. Ayala (Eds) Molecular Evolution Sinauer Sunderland 179–199
R. Hinegardner D.E. Rosen (1972) ArticleTitleCellular DNA content and the evolution of teleostean fishes Am. Naturalist 106 621–644 Occurrence Handle1:CAS:528:DyaE38Xls1ahs78%3D Occurrence Handle10.1086/282801
Holland, P.W., J. Garcia-Fernandez, J.W. Williams & A. Sidow, 1994. Gene duplications and the origins of vertebrate development. Development supplement: 125–133
O. Jaillon 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 R. Anthouard C. Jubin V. Castelli M. Katinka B. Vacherie C. Biemont Z. Skalli L. Cattolico J. Poulain V. Berardinis Particlede 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. Guigo M.C. Zody J. Mesirov K. Lindblad-Toh B. Birren C. Nusbaum D. Kahn M. Robinson-Rechavi V. Laudet V. Schachter F. Quetier W. Saurin C. Scarpelli P. Wincker E.S. Lander J. Weissenbach H.R. Crollius (2004) ArticleTitleGenome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype Nature 431 946–957 Occurrence Handle15496914 Occurrence Handle10.1038/nature03025
K. Kawakami T. Noda (2004) ArticleTitleTransposition of the Tol2 element, an Ac-like element from the Japanese medaka fish Oryzias latipes, in mouse embryonic stem cells Genetics 166 895–899 Occurrence Handle15020474 Occurrence Handle1:CAS:528:DC%2BD2cXjtlyntLw%3D Occurrence Handle10.1534/genetics.166.2.895
K. Kawakami A. Shima N. Kawakami (2000) ArticleTitleIdentification of a functional transposase of the Tol2 element, an Ac-like element from the Japanese medaka fish, and its transposition in the zebrafish germ lineage Proc. Natl. Acad. Sci. USA 97 11403–11408 Occurrence Handle11027340 Occurrence Handle1:CAS:528:DC%2BD3cXnsF2qsr4%3D Occurrence Handle10.1073/pnas.97.21.11403
D. Larhammar C. Risinger (1994) ArticleTitleMolecular genetic aspects of tetraploidy in the common carp, Cyprinus carpio Mol. Phylogenet. Evol. 3 59–68 Occurrence Handle8025730 Occurrence Handle1:CAS:528:DyaK2cXltVClsL8%3D Occurrence Handle10.1006/mpev.1994.1007
D.R. Maddison W.P. Maddison (2000) MacClade 4: Analysis of Phylogeny and Character Evolution Sinauer Sunderland, MA
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: 33–38
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: 83–93
J.E. Mank D.E.L. Promislow J.C. Avise (2005) ArticleTitlePhylogenetic perspectives on the evolution of parental care in fishes Evolution 59 1570–1578 Occurrence Handle16153042 Occurrence Handle10.1554/04-734
A. Meyer E. Malaga-Trillo (1999) ArticleTitleVertebrate genomics: more fishy tales about Hox genes Curr. Biol. 9 r210–r213 Occurrence Handle10209088 Occurrence Handle1:CAS:528:DyaK1MXitFGitrY%3D Occurrence Handle10.1016/S0960-9822(99)80131-6
A. Meyer M. Schartl (1999) ArticleTitleGene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions Curr. Opin. Cell Biol. 11 699–704 Occurrence Handle10600714 Occurrence Handle1:CAS:528:DyaK1MXotVKjsb0%3D Occurrence Handle10.1016/S0955-0674(99)00039-3
A. Navarro N.H. Barton (2003a) ArticleTitleAccumulating postzygotic isolation gene in parapatry: a new twist on chromosomal speciation Evolution 57 447–459 Occurrence Handle10.1554/0014-3820(2003)057[0447:APIGIP]2.0.CO;2
A. Navarro N.H. Barton (2003b) ArticleTitleChromosomal speciation and molecular divergence – accelerated evolution in rearranged chromosomes Science 300 321–324 Occurrence Handle1:CAS:528:DC%2BD3sXislyqtLs%3D Occurrence Handle10.1126/science.1080600
D.E. Neafsey S.R. Palumbi (2003) ArticleTitleGenome size evolution in pufferfish: a comparative analysis of diodontid and tetraodontid pufferfish genomes Genome Res. 13 821–839 Occurrence Handle12727902 Occurrence Handle1:CAS:528:DC%2BD3sXjs1Oqtbc%3D Occurrence Handle10.1101/gr.841703
S. Ohno (1967) Sex Chromosomes and Sex-Linked Genes Springer-Verlag New York
C. Ozouf-Costaz J. Brandt C. Korting E. Pisano C. Bonillo J.P. Coutanceau J.-N. Volff (2004) ArticleTitleGenome dynamics and chromosomal localization of the non-LTR retrotransposons Rex1 and Rex3 in Antarctic fish Antarctic Sci. 16 51–57 Occurrence Handle10.1017/S0954102004001816
J.H. Postlethwait I.G. Woods P. Ngo-Hazelett Y.L. Yan P.D. Kelly F. Chu H. Huang A. Hill-Force W.S. Talbot (2002) ArticleTitleZebrafish comparative genomics and the origins of vertebrate chromosomes Genome Res. 10 1890–1902 Occurrence Handle10.1101/gr.164800
M. Robinson-Rechavi V. Laudet (2001) ArticleTitleEvolutionary rates of duplicate genes in fish and mammals Mol. Biol. Evol. 18 681–683 Occurrence Handle11264421 Occurrence Handle1:CAS:528:DC%2BD3MXis1eitrs%3D
M. Robinson-Rechavi O. Marchand H. Schriva P.L. Bardet D. Zelus S. Hughes V. Laudet (2001) ArticleTitleEuteleost fish genomes are characterized by expansions of gene families Genome Res. 11 781–788 Occurrence Handle11337474 Occurrence Handle1:CAS:528:DC%2BD3MXjs1Wmurg%3D Occurrence Handle10.1101/gr.165601
S.F. Smith P. Snell F. Gruetzner A.J. Bench T. Haaf J.A. Metcalfe A.R. Green G. Elgar (2002) ArticleTitleAnalysis of the extent of shared synteny and conserved gene orders between the genome of Fugu rupripes and human 20q Genome Res. 12 776–784 Occurrence Handle11997344 Occurrence Handle1:CAS:528:DC%2BD38XjvFSgtLo%3D Occurrence Handle10.1101/gr.221802. Article published online before print in April 2002
R.R. Sokal F.J. Rohlf (1995) Biometry: The Principle and Practice of Statistics in Biology Research Freemand and Co New York
S.G. Stephens (1951) ArticleTitlePossible significance of duplications in evolution Adv. Genet. 4 247–265 Occurrence Handle14943679 Occurrence Handle1:STN:280:Cy2D2sznvV0%3D Occurrence Handle10.1016/S0065-2660(08)60237-0
J.W. Thomas J.W. Touchman R.W. Blakesley G.G. Bouffard S.M. Beckstrom-Sternberg E.H. Margulies M. Blanchette A.C. Siepel P.J. Thomas J.C. McDowell B. Maskeri N.F. Hansen M.S. Schwartz R.J. Weber W.J. Kent D. Karolchik T.C. Bruen R. Bevan D.J. Cutler S. Schwartz L. Elnitski J.R. Idol A.B. Prasad S.Q. Lee-Lin V.V.B. Maduro T.J. Summers M.E. Portnoy N.L. Dietrich N. Akhter K. Ayele B. Benjamin K. Cariaga C.P. Brinkley S.Y. Brooks S. Granite X. Guan J. Gupta P. Haghighi S.L. Ho M.C. Huang E. Karlins P.L. Laric R. Legaspi M.J. Lim Q.L. Maduro C.A. Masiello S.D. Mastrian J.C. McCloskey R. Pearson S. Stantripop E.E. Tiongson J.T. Tran C. Tsurgeon J.L. Vogt M.A. Walker K.D. Wetherby L.S. Wiggins A.C. Young L.H. Zhang K. Osoegawa B. Zhu B. Zhao C.L. Shu P.J. Jong ParticleDe C.E. Lawrence A.F. Smit A. Chakravarti D. Haussler P. Green W. Miller E.D. Green (2003) ArticleTitleComparative analyses of multi-species sequences from targeted genomic regions Nature 424 788–793 Occurrence Handle12917688 Occurrence Handle1:CAS:528:DC%2BD3sXmt1antrs%3D Occurrence Handle10.1038/nature01858
T. Uyeno G.R. Smith (1972) ArticleTitleTetraploid origin of the karyotype of catostomid fishes Science 175 644–646 Occurrence Handle5009763 Occurrence Handle1:STN:280:CS2D1Mfis1M%3D
V.P. Vasil’ev (1999) ArticleTitlePolyploidization by reticular speciation in acipenseriform evolution: a working hypothesis J. Appl. Ichthyol. 15 29–31 Occurrence Handle10.1046/j.1439-0426.1999.00096.x
B. Venkatesh (2003) ArticleTitleEvolution and diversity of fish genomes Curr. Opin. Genet. Develop. 13 588–592 Occurrence Handle1:CAS:528:DC%2BD3sXpt1SnsLg%3D Occurrence Handle10.1016/j.gde.2003.09.001
J.-N. Volff (2005) ArticleTitleGenome evolution and biodiversity in teleost fish Heredity 94 280–294 Occurrence Handle15674378 Occurrence Handle1:CAS:528:DC%2BD2MXhsFOqtbw%3D Occurrence Handle10.1038/sj.hdy.6800635
J. Wittbrodt A. Meyer M. Schartl (1998) ArticleTitleMore genes in fish? Bioessays 20 511–512 Occurrence Handle10.1002/(SICI)1521-1878(199806)20:6<511::AID-BIES10>3.0.CO;2-3
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mank, J.E., Avise, J.C. Phylogenetic conservation of chromosome numbers in Actinopterygiian fishes. Genetica 127, 321–327 (2006). https://doi.org/10.1007/s10709-005-5248-0
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10709-005-5248-0