Sequence analyses of the distal-less homeobox gene family in East African cichlid fishes reveal signatures of positive selection
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  • 作者:Eveline T Diepeveen (10)
    Fabienne D Kim (10)
    Walter Salzburger (10)
  • 关键词:Distal ; less homeobox gene ; Molecular evolution ; Cichlid fishes ; Teleost fishes ; Positive selection ; Differential selection ; Gene duplication ; dN/dS
  • 刊名:BMC Evolutionary Biology
  • 出版年:2013
  • 出版时间:December 2013
  • 年:2013
  • 卷:13
  • 期:1
  • 全文大小:952KB
  • 参考文献:1. Meyer A, Van de Peer Y: From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). / Bioessays 2005, 27:937-45. CrossRef
    2. Volff JN: Genome evolution and biodiversity in teleost fish. / Heredity 2005, 94:280-94. CrossRef
    3. Taylor JS, Braasch I, Frickey T, Meyer A, Van de Peer Y: Genome duplication, a trait shared by 22,000 species of ray-finned fish. / Genome Res 2003, 13:382-90. CrossRef
    4. Taylor JS, Van de Peer Y, Braasch I, Meyer A: Comparative genomics provides evidence for an ancient genome duplication event in fish. / Phil Trans R Soc Lond B 2001, 356:1661-679. CrossRef
    5. Ohno S: / Evolution by gene duplication. New York: Springer Verlag; 1970.
    6. Santini F, Harmon LJ, Carnevale G, Alfaro ME: Did genome duplication drive the origin of teleosts? A comparative study of diversification in ray-finned fishes. / BMC Evol Biol 2009, 9:194. CrossRef
    7. De Rosa R, Grenier JK, Andreevas T, Cook CE, Adoutte A, Akam M, Carroll SB, Balavoine G: Hox genes in brachiopods and priapulids and protostome evolution. / Nature 1999, 399:772-76. CrossRef
    8. Lemons D, McGinnis W: Genomic evolution of Hox gene clusters. / Science 2006, 313:1918-922. CrossRef
    9. Ruddle FH, Bartels JL, Bentley KL, Kappen C, Murtha MT, Pendleton JW: Evolution of Hox genes. / Annu Rev Genet 1994, 28:423-42. CrossRef
    10. Gehring WJ, Hiromi Y: Homeotic genes and the homeobox. / Annu Rev Genet 1986, 20:147-73. CrossRef
    11. Cohn MJ, Tickle C: Limbs: a model for pattern formation within the vertebrate body plan. / Trends Genet 1996, 12:253-57. CrossRef
    12. Zakany J, Duboule D: The role of Hox genes during vertebrate limb development. / Curr Opin Genet Dev 2007, 17:359-66. CrossRef
    13. Weatherbee SD, Nijhout HF, Grunert LW, Halder G, Galant R, Selegue J, Carroll SB: Ultrabithorax function in butterfly wings and the evolution of insect wing patterns. / Curr Biol 1999, 9:109-15. CrossRef
    14. Warren RW, Nagy L, Selegue J, Gates J, Carroll SB: Evolution of homeotic gene regulation and function in flies and butterflies. / Nature 1994, 372:458-61. CrossRef
    15. Pick L, Heffer A: Hox gene evolution: multiple mechanisms contributing to evolutionary novelties. / Ann N Y Acad Sci 2012, 1256:15-2. CrossRef
    16. Pearson JC, Lemons D, McGinnis W: Modulating Hox gene functions during animal body patterning. / Nat Rev Genet 2005, 6:893-04. CrossRef
    17. Seehausen O: African cichlid fish: a model system in adaptive radiation research. / Proc R Soc B 2006, 273:1987-998. CrossRef
    18. Salzburger W: The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes. / Mol Ecol 2009, 18:169-85. CrossRef
    19. Kornfield I, Smith PF: African cichlid fishes: model systems for evolutionary biology. / Annu Rev Ecol Syst 2000, 31:163-96. CrossRef
    20. Kocher TD: Adaptive evolution and explosive speciation: the cichlid fish model. / Nat Rev Genet 2004, 5:288-98. CrossRef
    21. Santos ME, Salzburger W: How cichlids diversify. / Science 2012, 338:619-21. CrossRef
    22. Turner GF, Seehausen O, Knight ME, Allender CJ, Robinson RL: How many species of cichlid fishes are there in African lakes? / Mol Ecol 2001, 10:793-06. CrossRef
    23. Genner MJ, Seehausen O, Lunt DH, Joyce DA, Shaw PW, Carvalho GR, Turner GF: Age of cichlids: new dates for ancient lake fish radiations. / Mol Biol Evol 2007, 24:1269-282. CrossRef
    24. Verheyen E, Salzburger W, Snoeks J, Meyer A: Origin of the superflock of cichlid fishes from Lake Victoria, East Africa. / Science 2003, 300:325-29. CrossRef
    25. Barlow GW: / The cichlid fishes: nature’s grand experiment in evolution. Cambridge: Perseus publishing; 2000.
    26. Coulter GW: / Lake Tanganyika and its life. Oxford: British Museum (Natural History) and Oxford University Press; 1991.
    27. Fryer G, Iles TD: / The cichlid fishes of the Great Lakes of Africa: their biology and Evolution. Edinburgh: Oliver & Boyd; 1972:1-34.
    28. Liem KF: Evolutionary strategies and morphological innovations: Cichlid pharyngeal jaws. / Systematic Zoology 1973, 22:425-41. CrossRef
    29. Muschick M, Indermaur A, Salzburger W: Convergent evolution within an adaptive radiation of cichlid fishes. / Curr Biol 2012, 22:2362-368. CrossRef
    30. Salzburger W, Mack T, Verheyen E, Meyer A: Out of Tanganyika: Genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes. / BMC Evol Biol 2005, 5:17. CrossRef
    31. Salzburger W, Braasch I, Meyer A: Adaptive sequence evolution in a color gene involved in the formation of the characteristic egg-dummies of male haplochromine cichlid fishes. / BMC Biol 2007, 5:51. CrossRef
    32. Roberts RB, Ser JR, Kocher TD: Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi cichlid fishes. / Science 2009, 326:998-001. CrossRef
    33. Fraser GJ, Hulsey CD, Bloomquist RF, Uyesugi K, Manley NR, Streelman JT: An ancient gene network is co-opted for teeth on old and new jaws. / Plos Biol 2009, 7:e31. CrossRef
    34. Fraser GJ, Bloomquist RF, Streelman JT: A periodic pattern generator for dental diversity. / BMC Biol 2008, 6:32. CrossRef
    35. Renz AJ, Gunter HM, Fischer JM, Qiu H, Meyer A, Kuraku S: Ancestral and derived attributes of the dlx gene repertoire, cluster structure and expression patterns in an African cichlid fish. / EvoDevo 2011, 2:1. CrossRef
    36. Diepeveen ET, Salzburger W: Molecular characterization of two endothelin pathways in East African cichlid fishes. / J Mol Evol 2011, 73:355-68. CrossRef
    37. Kuraku S, Meyer A: Genomic analysis of cichlid fish ‘natural mutants- / Curr Opin Genet Dev 2008, 18:551-58. CrossRef
    38. Parichy DM, Ransom DG, Paw B, Zon LI, Johnson SL: An orthologue of the kit -related gene fms is required for development of neural crest-derived xanthophores and a subpopulation of adult melanocytes in the zebrafish, Danio rerio . / Development 2000, 127:3031-044.
    39. Parichy DM, Turner JM: Temporal and cellular requirements for Fms signaling during zebrafish adult pigment pattern development. / Development 2003, 130:817-33. CrossRef
    40. Albertson RC, Streelman JT, Kocher TD, Yelick PC: Integration and evolution of the cichlid mandible: the molecular basis of alternate feeding strategies. / P Natl Acad Sci Usa 2005, 102:16287-6292. CrossRef
    41. Hoegg S, Boore JL, Kuehl JV, Meyer A: Comparative phylogenomic analyses of teleost fish Hox gene clusters: lessons from the cichlid fish Astatotilapia burtoni . / BMC Genomics 2007, 8:317. CrossRef
    42. Panganiban G, Rubenstein J: Developmental functions of the Distal-less /Dlx homeobox genes. / Development 2002, 129:4371-386.
    43. Ellies DL, Stock DW, Hatch G, Giroux G, Weiss KM, Ekker M: Relationship between the genomic organization and the overlapping embryonic expression patterns of the zebrafish dlx genes. / Genomics 1997, 45:580-90. CrossRef
    44. Borday-Birraux V, Van der Heyden C, Debiais-Thibaud M, Verreijdt L, Stock DW, Huysseune A, Sire J-Y: Expression of Dlx genes during the development of the zebrafish pharyngeal dentition: evolutionary implications. / Evol Dev 2006, 8:130-41. CrossRef
    45. Debiais-Thibaud M, Germon I, Laurenti P, Casane D, Borday-Birraux V: Low divergence in Dlx gene expression between dentitions of the medaka ( Oryzias latipes ) versus high level of expression shuffling in osteichtyans. / Evol Dev 2008, 10:464-76. CrossRef
    46. Beldade P, Brakefield PM, Long AD: Contribution of Distal-less to quantitative variation in butterfly eyespots. / Nature 2002, 415:315-18. CrossRef
    47. Reed RD, Serfas MS: Butterfly wing pattern evolution is associated with changes in a Notch/Distal-less temporal pattern formation process. / Curr Biol 2004, 14:1159-166. CrossRef
    48. Brakefield PM, Gates J, Keys D, Kesbeke F, Wijngaarden PJ, Monteiro A, French V, Carroll SB: Development, plasticity and evolution of butterfly eyespot patterns. / Nature 1996, 384:236-42. CrossRef
    49. Sunkel CE, Whittle J: Brista : A gene involved in the specification and differentiation of distal cephalic and thoracic structures in Drosophila melanogaster . / Roux’s Arch Dev Biol 1987, 196:124-32. CrossRef
    50. Dong P, Chu J, Panganiban G: Coexpression of the homeobox genes Distal-less and homothorax determines Drosophila antennal identity. / Development 2000, 127:209-16.
    51. Gordon CT, Brinas I, Rodda FA, Bendall AJ, Farlie PG: Role of Dlx genes in craniofacial morphogenesis: Dlx2 influences skeletal patterning by inducing ectomesenchymal aggregation in ovo. / Evol Dev 2010, 12:459-73. CrossRef
    52. Stock DW, Ellies DL, Zhao ZY, Ekker M, Ruddle FH, Weiss KM: The evolution of the vertebrate Dlx gene family. / P Natl Acad Sci Usa 1996, 93:10858-0863. CrossRef
    53. Terai Y, Morikawa N, Okada N: The evolution of the pro-domain of bone morphogenetic protein 4 ( Bmp4 ) in an explosively speciated lineage of East African cichlid fishes. / Mol Biol Evol 2002, 19:1628-632. CrossRef
    54. Notredame C, Higgins DG, Heringa J: T-Coffee: a novel method for fast and accurate multiple sequence alignment. / J Mol Biol 2000, 302:205-17. CrossRef
    55. Poirot O, O’Toole E: Tcoffee@igs: a web server for computing, evaluating and combining multiple sequence alignments. / Nucleic Acids Res 2003, 31:3503-506. CrossRef
    56. Swofford DL: / Phylogenetic Analysis Using Parsimony (*and Other Methods). Sunderland: Sinauer Associates; 2003.
    57. / Geneious version 5.6 created by Biomatters. Available from http://www.geneious.com/
    58. Bruford MW, Hanotte O, Brookfield J, Burke T: Multilocus and single-locus DNA fingerprinting. In / Molecular genetic analysis of populations: a practical approach. Edited by: Hoelzel AR. Oxford: Oxford University Press; 1998:287-36.
    59. Huelsenbeck JP, Ronquist F: MRBAYES: Bayesian inference of phylogeny. / Bioinformatics 2001, 17:754-55. CrossRef
    60. Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. / Bioinformatics 2003, 19:1572-574. CrossRef
    61. Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum-likelihood. / Syst Biol 2003, 52:696-04. CrossRef
    62. Posada D: jModelTest: phylogenetic model averaging. / Mol Biol Evol 2008, 25:1253-256. CrossRef
    63. Salzburger W, Meyer A, Baric S, Verheyen E, Sturmbauer C: Phylogeny of the Lake Tanganyika cichlid species flock and its relationship to the Central and East African haplochromine cichlid fish faunas. / Systematic Biology 2002, 51:113-35. CrossRef
    64. Yang Z: PAML, A program package for phylogenetic analysis by maximum likelihood. / Comput Appl Biosci 1997, 13:555-56.
    65. Yang Z: PAML 4: phylogenetic analysis by maximum likelihood. / Mol Biol Evol 2007, 24:1586-591. CrossRef
    66. Nielsen R, Yang Z: Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. / Genetics 1998, 148:929-36.
    67. Yang Z, Nielsen R, Goldman N: Codon- substitution models for heterogeneous selection pressure at amino acid sites. / Genetics 2000, 155:431-49.
    68. Yang Z, Wong W, Nielsen R: Bayes empirical Bayes inference of amino acid sites under positive selection. / Mol Biol Evol 2005, 22:1107-118. CrossRef
    69. Kosakovsky Pond SL, Frost S, Muse SV: HyPhy: hypothesis testing using phylogenies. / Bioinformatics 2005, 22:676-79. CrossRef
    70. Massingham T, Goldman N: Detecting amino acid sites under positive selection and purifying selection. / Genetics 2005, 169:1753-762. CrossRef
    71. Ng P, Henikoff ST: SIFT: predicting amino acid changes that affect protein functions. / Nucleic Acids Research 2003, 31:3812-814. CrossRef
    72. Star B, Nederbragt AJ, Jentoft S, Grimholt U, Malmstr?m M, Gregers TF, Rounge TB, Paulsen J, Solbakken MH, Sharma A, Wetten OF, Lanzén A, Winer R, Knight J, Vogel J-H, Aken B, Andersen ?, Lagesen K, Tooming-Klunderud A, Edvardsen RB, Tina KG, Espelund M, Nepal C, Previti C, Karlsen BO, Moum T, Skage M, Berg PR, Gj?en T, Kuhl H, / et al.: The genome sequence of Atlantic cod reveals a unique immune system. / Nature 2011, 477:207-10. CrossRef
    73. Sumiyama K, Irvine SQ, Stock DW, Weiss KM, Kawasaki K, Shimizu N, Shashikant CS, Miller W, Ruddle FH: Genomic structure and functional control of the Dlx3- bigene cluster. / P Natl Acad Sci Usa 2002, 99:780-85. CrossRef
    74. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J: Preservation of duplicate genes by complementary, degenerative mutations. / Genetics 1999, 151:1531-545.
    75. Sidow A: Gen(om)e duplications in the evolution of early vertebrates. / Curr Opin Genet Dev 1996, 6:715-22. CrossRef
    76. Ohta T: Simulating evolution by gene duplication. / Genetics 1987, 115:207-13.
    77. Marotta M, Piontkivska H, Tanaka H: Molecular trajectories leading to the alternative fates of duplicate genes. / PLoS ONE 2012, 7:e38958. CrossRef
    78. Conrad B, Antonarakis SE: Gene duplication: a drive for phenotypic diversity and cause of human disease. / Annu Rev Genom Human Genet 2007, 8:17-5. CrossRef
    79. Prince VE, Pickett FB: Splitting pairs: the diverging fates of duplicated genes. / Nature Reviews Genetics 2002, 3:827-37. CrossRef
    80. Braasch I, Volff JN, Schartl M: The endothelin system: evolution of vertebrate-specific ligand-receptor interactions by three rounds of genome duplication. / Mol Biol Evol 2009, 26:783-99. CrossRef
    81. Zhang J, Zhang Y-P, Rosenberg HF: Adaptive evolution of a duplicated pancreatic ribonuclease gene in a leaf-eating monkey. / Nat Genet 2002, 30:411-15. CrossRef
    82. Zhang J: Parallel adaptive origins of digestive RNases in Asian and African leaf monkeys. / Nat Genet 2006, 38:819-23. CrossRef
    83. Dermitzakis ET, Clark AG: Differential selection after duplication in mammalian developmental genes. / Mol Biol Evol 2001, 18:557-62. CrossRef
    84. Terai Y, Morikawa N, Kawakami K, Okada N: Accelerated evolution of the surface amino acids in the WD-repeat domain encoded by the hagoromo gene in an explosively speciated lineage of east African cichlid fishes. / Mol Biol Evol 2002, 19:574-78. CrossRef
    85. Wagner GP, Lynch VJ: Evolutionary novelties. / Current Biology 2010, 20:R48-R52. CrossRef
    86. Prud’homme B, Gompel N, Carroll SB: Emerging principles of regulatory evolution. / P Natl Acad Sci Usa 2007, 104:8605-612. CrossRef
  • 作者单位:Eveline T Diepeveen (10)
    Fabienne D Kim (10)
    Walter Salzburger (10)

    10. Zoological Institute, University of Basel, Vesalgasse 1, 4051, Basel, Switzerland
文摘
Background Gen(om)e duplication events are hypothesized as key mechanisms underlying the origin of phenotypic diversity and evolutionary innovation. The diverse and species-rich lineage of teleost fishes is a renowned example of this scenario, because of the fish-specific genome duplication. Gene families, generated by this and other gene duplication events, have been previously found to play a role in the evolution and development of innovations in cichlid fishes - a prime model system to study the genetic basis of rapid speciation, adaptation and evolutionary innovation. The distal-less homeobox genes are particularly interesting candidate genes for evolutionary novelties, such as the pharyngeal jaw apparatus and the anal fin egg-spots. Here we study the dlx repertoire in 23 East African cichlid fishes to determine the rate of evolution and the signatures of selection pressure. Results Four intact dlx clusters were retrieved from cichlid draft genomes. Phylogenetic analyses of these eight dlx loci in ten teleost species, followed by an in-depth analysis of 23 East African cichlid species, show that there is disparity in the rates of evolution of the dlx paralogs. Dlx3a and dlx4b are the fastest evolving dlx genes, while dlx1a and dlx6a evolved more slowly. Subsequent analyses of the nonsynonymous-synonymous substitution rate ratios indicate that dlx3b, dlx4a and dlx5a evolved under purifying selection, while signs of positive selection were found for dlx1a, dlx2a, dlx3a and dlx4b. Conclusions Our results indicate that the dlx repertoire of teleost fishes and cichlid fishes in particular, is shaped by differential selection pressures and rates of evolution after gene duplication. Although the divergence of the dlx paralogs are putative signs of new or altered functions, comparisons with available expression patterns indicate that the three dlx loci under strong purifying selection, dlx3b, dlx4a and dlx5a, are transcribed at high levels in the cichlids-pharyngeal jaw and anal fin. The dlx paralogs emerge as excellent candidate genes for the development of evolutionary innovations in cichlids, although further functional analyses are necessary to elucidate their respective contribution.

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