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Evolutionary Genomics of Hox Gene Clusters

  • Sonja J. Prohaska
  • Peter F. Stadler
  • Günter P. Wagner

Abstract

The evolution of Hox clusters in vertebrates follows different patterns than those of in-vertebrate clusters. More stringent structural constraints in vertebrates are apparent from tighter cluster organization and the systematic expulsion of repetitive material. We speculate that the tendency of vertebrates to maintain Hox clusters after genome duplications might be related to these stricter constraints. Duplications may temporarily lift these constraints, thereby opening a window of adaptive opportunity for functional differentiation of the Hox genes that eventually leads to their fixation.

Keywords

Genome Duplication Paralog Group HoxD Cluster Oikopleura Dioica Noncoding Sequence Conservation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Gehring WJ. Master Control genes in development and evolution: The Homeobox story (Terry Lecture Series). New Haven: Yale University Press, 1998.Google Scholar
  2. 2.
    Cuvier G. Le régne animal; distribué d’après son organisation; pour servir de base à l’histoire naturelle des animaux et d’introduction à l’anatomie comparée. Deterville, Paris: 1817:4.Google Scholar
  3. 3.
    Powers TP, Hogan J, Ke Z et al. Characterization of the hox cluster from the mosquito anopheles gambiae (diptera: Culicidae). Evol Dev 2000; 2(6):311–325.PubMedCrossRefGoogle Scholar
  4. 4.
    Shashikant CS, Utset MF, Violette TL et al. Homeobox genes in mouse development. Crit Rev Eukaryot Gene Expr 1991; 1:207–245.PubMedGoogle Scholar
  5. 5.
    Pendleton J, Nagai BK, Murtha MT et al. Expansion of the Hox gene family and the evolution of chordates. Proc Natl Acad Sci USA 1993; 90:6300–6304.PubMedCrossRefGoogle Scholar
  6. 6.
    Murtha MT, Lcckman JF, Ruddle FH. Detection of homeobox genes in development and evolution. Proc Natl Acad Sci USA 1991; 88(23):10711–10715.PubMedCrossRefGoogle Scholar
  7. 7.
    Ferrier DEK, Minguillón C, Holland PWH et al. The amphioxus Hox cluster: Deuterostome posterior flexibility and Hox14. Evol Dev 2000; 2:284–293.PubMedCrossRefGoogle Scholar
  8. 8.
    Amores A, Force A, Yan YL et al. Postlethwait. Zebrafish hox clusters and vertebrate genome evolution. Science 1998; 282:1711–1714.PubMedCrossRefGoogle Scholar
  9. 9.
    Amores A, Suzuki T, Yan YL et al. Developmental roles of pufferfish hox clusters and genome evolution in ray-fin fish. Genome Res 2004; 14(1):1–10.PubMedCrossRefGoogle Scholar
  10. 10.
    Donoghue PCJ, Purnell MA. Genome duplication, extinction, and vertebrate evolution. Trends Ecol Evol 2005; 20:312–319.PubMedCrossRefGoogle Scholar
  11. 11.
    Crow KD, Stadler PF, Lynch VJ et al. The fish-specific hox cluster duplication is coincident with the origin of teleosts. Mol Biol Evol 2006; 23(1):121–136.PubMedCrossRefGoogle Scholar
  12. 12.
    Carroll SB, Weatherbee SD, Langeland JA. Homeotic genes and the regulation and evolution of insect wing number. Nature 1995; 375:58–61.PubMedCrossRefGoogle Scholar
  13. 13.
    Lynch VJ, Roth JJ, Takahashi T et al. Adaptive evolution of hoxa-11 and hoxa-13 at the origin of the uterus in mammals. Proc Biol Sci 2004; 271(1554):2201–2207.PubMedCrossRefGoogle Scholar
  14. 14.
    Cannatella DC, De Sá RO. Xenopus laevis as a model organism. Syst Biol 1993; 42:476–507.CrossRefGoogle Scholar
  15. 15.
    Johnson KR, Wright JE, May B. Linkage relationships reflecting ancestral tetraploidy in salmonid fish. Genetics 1987; 116(4):579–591.PubMedGoogle Scholar
  16. 16.
    Moghadam HK, Ferguson MM, Danzmann RG. Evidence for Hox gene duplication in rainbow trout (Oncorhynchus mykiss): A tetraploid model species. J Mol Evol 2005; 61:804–818.PubMedCrossRefGoogle Scholar
  17. 17.
    Moghadam HK, Ferguson MM, Danzmann RG. Evolution of Hox clusters in salmonidae: A comparative analysis between atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss). J Mol Evol 2005; 61:636–649.PubMedCrossRefGoogle Scholar
  18. 18.
    Wagner GP, Amemiya C, Ruddle F. Hox cluster duplications and the opportunity for evolutionary novelties. Proc Natl Acad Sci USA 2003; 100:14603–14606.PubMedCrossRefGoogle Scholar
  19. 19.
    Crow KD, Wagner GP. What is the role of genome duplication in the evolution of complexity and diversity? Mol Biol Evol 2006; 23:887–892.PubMedCrossRefGoogle Scholar
  20. 20.
    Garcia-Fernández J, Holland PW. Archetypal organization of the amphioxus hox gene cluster. Nature 1994; 370:563–566.PubMedCrossRefGoogle Scholar
  21. 21.
    Aboobaker AA. Hox gene loss during dynamic evolution of the nematode cluster. Curr Biol 2003; 13:37–40.PubMedCrossRefGoogle Scholar
  22. 22.
    Aboobaker A, Blaxter M. Hox gene evolution in nematodes: Novelty conserved. Curr Op Genet Devel 2003; 13:593–598.CrossRefGoogle Scholar
  23. 23.
    Negre B, Ranz JM, Casals F et al. A new split of the hox gene complex in drosophila: Relocation and evolution of the gene labial. Mol Biol Evol 2003; 20:2042–2054.PubMedCrossRefGoogle Scholar
  24. 24.
    Negre B, Casillas S, Suzanne M et al. Conservation of regulatory sequences and gene expression patterns in the disintegrating Drosophila Hox gene complex. Genome Res 2005; 15:692–700.PubMedCrossRefGoogle Scholar
  25. 25.
    Yasukochi Y, Ashakumary LA, Wu C et al. Organization of the Hox gene cluster of the silkworm, Bombyx mori: A split of the Hox cluster in a nonDrosophila insect. Dev Genes Evol 2004; 214:606–614.PubMedCrossRefGoogle Scholar
  26. 26.
    Pierce RJ, Wu W, Hirai H et al. Evidence for a dispersed Hox gene cluster in the platyhelminth parasite Schistosoma mansoni. Mol Biol Evol 2005; 22:2491–2503.PubMedCrossRefGoogle Scholar
  27. 27.
    Cameron RA, Rowen L, Nesbitt R et al. Unusual gene order and organization of the sea urchin hox cluster. J Exp Zoolog B (Mol Dev Evol) 2006; 306:45–58.CrossRefGoogle Scholar
  28. 28.
    Spagnuolo A, Ristoratore F, Di Gregorio A et al. Unusual number and genomic organization of Hox genes in the tunicate Ciona intestinalis. Gene 2003; 309:71–79.PubMedCrossRefGoogle Scholar
  29. 29.
    Ikuta T, Yoshida N, Satoh N et al. Ciona intestinalis hox gene cluster: Its dispersed structure and residual colinear expression in development. Proc Natl Acad Sci USA 2004; 101:15118–15123.PubMedCrossRefGoogle Scholar
  30. 30.
    Ikuta T, Saiga H. Organization of hox genes in ascidians: Present, past, and future. Dev Dyn 2005; 233:382–389.PubMedCrossRefGoogle Scholar
  31. 31.
    Seo HC, Edvardsen RB, Maeland AD et al. Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 2004; 431:67–71.PubMedCrossRefGoogle Scholar
  32. 32.
    Edvardsen RB, Seo HC, Jensen MFJ et al. Remodelling of the homeobox gene complement in the tunicate Oikopleura dioica. Curr Biol 2005; 15:R12–R13.PubMedCrossRefGoogle Scholar
  33. 33.
    Chiu CH, Amemiya C, Dewar K et al. Molecular evolution of the HoxA cluster in the three major gnathostome lineages. Proc Natl Acad Sci USA 2002; 99:5492–5497.PubMedCrossRefGoogle Scholar
  34. 34.
    Santini S, Boore JL, Meyer A. Evolutionary conservation of regulatory elements in vertebrate Hox gene clusters. Genome Res 2003; 13:1111–1122.PubMedCrossRefGoogle Scholar
  35. 35.
    Kurosawa G, Takamatsu N, Takahashi M et al. Organization and structure of hox gene loci in medaka genome and comparison with those of pufferfish and zebrafish genomes. Gene 2006; 370:75–82.PubMedCrossRefGoogle Scholar
  36. 36.
    Lee AP, Koh EG, Tay A et al. Highly conserved syntenic blocks at the vertebrate Hox loci and conserved regulatory elements within and outside hox gene clusters. Proc Natl Acad Sci USA 2006; 103:6994–6999.PubMedCrossRefGoogle Scholar
  37. 37.
    Fried C, Prohaska SJ, Stadler PF. Exclusion of repetitive DNA elements from gnathostome Hox clusters. J Exp Zool Mol Dev Evol 2004; 302B:165–173.CrossRefGoogle Scholar
  38. 38.
    Casals F, Caceres M, Ruiz A. The foldback-like transposon Galileo is involved in the generation of two different natural chromosomal inversions of Drosophila buzzatii. Mol Biol Evol 2003; 20:674–685.PubMedCrossRefGoogle Scholar
  39. 39.
    Lewis EB, Pfeiffer BD, Mathog DR et al. Evolution of the homeobox complex in Diptera. Curr Biol 2003; R587–R588.Google Scholar
  40. 40.
    Britten RJ. DNA sequence insertion and evolutionary variation in gene regulation. Proc Natl Acad Sci USA 1996; 93:9374–9377.PubMedCrossRefGoogle Scholar
  41. 41.
    Stenger JE, Lobachev KS, Gordenin D et al. Biased distribution of inverted and direct Alus in the human genome: Implications for insertion, exclusion, and genome stability. Genome Res 2001; 11:12–27.PubMedCrossRefGoogle Scholar
  42. 42.
    Okazaki Y, Furuno M, Kasukawa T et al. Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature 2002; 420:563–573.PubMedCrossRefGoogle Scholar
  43. 43.
    Imanishi T, Itoh T, Suzuki Y et al. Integrative annotation of 21,037 human genes validated by full-length cDNA clones. PLoS Biology 2004; 2:0856–0875.CrossRefGoogle Scholar
  44. 44.
    Bertone P, Stoc V, Royce TE et al. Snyder. Global identification of human transcribed sequences with genome tiling arrays. Science 2004; 306:2242–2246.PubMedCrossRefGoogle Scholar
  45. 45.
    Kampa D, Cheng J, Kapranov P et al. Novel RNAs identified from an in-depth analysis of the transcriptome of human chromosomes 21 and 22. Genome Res 2004; 14:331–342.PubMedCrossRefGoogle Scholar
  46. 46.
    Johnson JM, Edwards S, Shoemaker D et al. Dark matter in the genome: Evidence of widespread transcription detected by microarray tiling experiments. Trends Genet 2005; 21:93–102.PubMedCrossRefGoogle Scholar
  47. 47.
    Cheng J, Kapranov P, Drenkow J et al. Transcriptional maps of 10 human chromosomes at 5-nucle-otide resolution. Science 2005; 308:1149–1154.PubMedCrossRefGoogle Scholar
  48. 48.
    Washietl S, Hofacker IL, Lukasser M et al. Mapping of conserved RNA secondary structures predicts thousands of functional noncoding RNAs in the human genome. Nature Biotech 2005; 23:1383–1390.CrossRefGoogle Scholar
  49. 49.
    Pedersen JS, Bejerano G, Siepel A et al. Identification and classification of conserved RNA secondary structures in the human genome. PLoS Comput Biol 2006; 2:e33.PubMedCrossRefGoogle Scholar
  50. 50.
    Benson DA, Karsch-Mizrachi I, Lipman D et al. GenBank: Update. Nucl Acids Res 2004; 32:D23–26.PubMedCrossRefGoogle Scholar
  51. 51.
    Sugnet CW, Kent WJ, M A et al. Transcriptome and genome conservation of alternative splicing events in humans and mice. Pacific Symp Biocomp 2004; 9:66–77.Google Scholar
  52. 52.
    RIKEN Genome Exploration Research Group. Antisense transcription in the mammalian transcriptome. Science 2005; 309:1564–1566.CrossRefGoogle Scholar
  53. 53.
    Potter SS, Brandford WW. Evolutionary conservation and tissue-specific processing of Hoxa 11 antisense transcripts. Mamm Genome 1998; 9:799–806.PubMedCrossRefGoogle Scholar
  54. 54.
    Michael Chau SPY, Taylor HS. HOXA11 silencing and endogenous HOXA11 antisense ribonucleic acid in the uterine endometrium. J Clin Endocrin Metabolism 2002; 87:2674–2680.CrossRefGoogle Scholar
  55. 55.
    Liu XF, Olsson P, Wolfgang CD et al. PRAC: A novel small nuclear protein that is specifically expressed in human prostate and colon. Prostate 2001; 47:125–131.PubMedCrossRefGoogle Scholar
  56. 56.
    Olsson P, Motegi A, Bera TK et al. PRAC2: A new gene expressed in human prostate and prostate cancer. Prostate 2003; 56:123–130.PubMedCrossRefGoogle Scholar
  57. 57.
    Tanzer A, Amemiya CT, Kim CB et al. Evolution of microRNAs located within Hox gene clusters. J Exp Zool Mol Dev Evol 2005; 304B:75–85.CrossRefGoogle Scholar
  58. 58.
    Chopra VS, Mishra RK. “mir”acles in Hox gene regulation. Bioessays 2006; 28:445–448.PubMedCrossRefGoogle Scholar
  59. 59.
    Hadrys T, Prince V, Hunter M et al. Comparative genomic analysis of vertebrate Hox3 and Hox4 genes. J Exp Zool B Mol Dev Evol 2004; 302:147–164.PubMedGoogle Scholar
  60. 60.
    Yekta S, Shih IH, Bartel DP. MircoRNA-directed cleavage of HoxB8 mRNA. Science 2004; 304:594–596.PubMedCrossRefGoogle Scholar
  61. 61.
    Irvine SQ, Carr JL, Bailey WJ et al. Genomic analysis of Hox clusters in the sea lamprey, Petromyzon marinus. J Exp Zool (Mol Dev Evol) 2002; 294:47–62.CrossRefGoogle Scholar
  62. 62.
    Ronshaugen M, Biemar F, Piel J et al. The drosophila microRNA iab-4 causes a dominant homeotic transformation of halteres to wings. Genes Dev 2005; 19:2947–2952.PubMedCrossRefGoogle Scholar
  63. 63.
    Delsuc F, Brinkmann H, Chourrout D et al. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 2006; 439(7079):923–924.CrossRefGoogle Scholar
  64. 64.
    Campos PRA, de Olivera VM, Wagner GP et al. Gene phylogenies and protein-protein interactions: Possible artifacts resulting from shared protein interaction partners. J Theor Biol 2004; 231:197–202.PubMedCrossRefGoogle Scholar
  65. 65.
    Misof BY, Wagner GP. Evidence for four hox clusters in the killifish fundulus heteroclitus (teleostei). Mol Phylogenet Evol 1996; 5(2):309–322.PubMedCrossRefGoogle Scholar
  66. 66.
    Misof BY, Blanco MJ, Wagner GP. PCR-survey of hox-genes of the zebrafish: New sequence information and evolutionary implications. J Exp Zool 1996; 274(3):193–206.PubMedCrossRefGoogle Scholar
  67. 67.
    Powers TP, Amemiya CT. Evidence for a hox14 paralog group in vertebrates. Current Biol 2004; 14:R183–R184.CrossRefGoogle Scholar
  68. 68.
    Janvier P. Early Vertebrates. Oxford: Clarendon Press, 1996.Google Scholar
  69. 69.
    Nelson JS. Fishes of the World. New York: John Wiley and Sons Inc., 1994.Google Scholar
  70. 70.
    Forey P, Janvier P. Agnathans and the origin of jawed vertebrates. Nature 1993; 361:129–134.CrossRefGoogle Scholar
  71. 71.
    Maisey JG. Heads and tails: A chordate phylogeny. Cladistics 1986; 2:201–256.CrossRefGoogle Scholar
  72. 72.
    Furlong RF, Holland PW. Bayesian phylogenetic analysis supports monophyly of ambulacria and cyclostomes. Zool Sci 2002; 19:593–599.PubMedCrossRefGoogle Scholar
  73. 73.
    Kuraku S, Hoshiyama K, Katoh D et al. Monophyly of lampreys and hagfishes supported by nuclear DNA-coded sequences. J Mol Evol 1999; 49:729–735.PubMedCrossRefGoogle Scholar
  74. 74.
    Mallatt J, Sullivan J. 28S and 18S rDNA sequences support the monophyly of lampreys and hagfishes. Mol Biol Evol 1998; 15:1706–1718.PubMedGoogle Scholar
  75. 75.
    Stock DW, Whitt GS. Evidence from 18S ribosomal RNA sequences that lampreys and hagfish form a natural group. Science 1992; 257:787–789.PubMedCrossRefGoogle Scholar
  76. 76.
    Delabre C, Gallut C, Barriel V et al. Complete mitochondrialDNA of the hagfish, Eptatretus burgerie: The comparative anaylsis of mitochondrial DNA sequences strongly supports cyclostome monophyly. Mol Phylog Evol 2002; 22:184–192.CrossRefGoogle Scholar
  77. 77.
    Takezaki N, Figueroa F, Zelska-Rutcynska Z et al. Molecular phylogeny of early vertebrates: Monophyly of the agnathans as revealed by sequences of 35 genes. Mol Biol Evol 2003; 20:287–292.PubMedCrossRefGoogle Scholar
  78. 78.
    Gűrsoy HC, Koper D, Benecke BJ. The vertebrate 7S K RNA separates hagfish (Myxine glutinosa) and lamprey (Lampetra fluviatilis). J Mol Evol 2000; 50:456–464.PubMedGoogle Scholar
  79. 79.
    Rasmussen AS, Janke A, Arnason U. The mitochondrial DNA molecule of the hagfish Myxine glutinosa and vertebrate phylogeny. J Mol Evol 1998; 46:382–388.PubMedCrossRefGoogle Scholar
  80. 80.
    Sharman AC, Holland PW. Estimation of Hox gene cluster number in lampreys. Int J Dev Biol 1998; 42:617–620.PubMedGoogle Scholar
  81. 81.
    Force A, Amores A, Postlethwait JH. Hox cluster organization in the jawless vertebrate Petromyzon marinus. J Exp Zool (Mol Dev Evol) 2002; 294:30–46.CrossRefGoogle Scholar
  82. 82.
    Fried C, Prohaska SJ, Stadler PF. Independent Hox-cluster duplications in lampreys. J Exp Zool Mol Dev Evol 2003; 299B:18–25.CrossRefGoogle Scholar
  83. 83.
    Takio Y, Pasqualetti M, Kuraku S et al. Evolutionary biology: Lamprey hox genes and the evolution of jaws. Nature 2004; 429:262f.CrossRefGoogle Scholar
  84. 84.
    Cohn MJ. Evolutionary biology: Lamprey Hox genes and the origin of jaws. Nature 2002; 416:386–387.PubMedCrossRefGoogle Scholar
  85. 85.
    Escriva H, Manzon L, Youson J et al. Analysis of lamprey and hagfish genes reveals a complex history of gene duplications during early vertebrate evolution. Mol Biol Evol 2002; 19:1440–1450.PubMedGoogle Scholar
  86. 86.
    Neidert AH, Virupannavar V, Hooker GW et al. Lamprey dlx genes and early vertebrate evolution. Proc Natl Acad Sci USA 2001; 98:1665–1670.PubMedCrossRefGoogle Scholar
  87. 87.
    Germot A, Lecointre G, Plouhinec JL et al. Structural evolution of otx genes in craniates. Mol Biol Evol 2001; 18:1668–1678.PubMedGoogle Scholar
  88. 88.
    Stadler PF, Fried C, Prohaska SJ et al. Evidence for independent Hox gene duplications in the hagfish lineage: A PCR-based gene inventory of Eptatretus stoutii. Mol Phylog Evol 2004; 32:686–692.CrossRefGoogle Scholar
  89. 89.
    Nieselt-Struwe K, von Haeseler A. Quartet-mapping, a generalization of the likelihood mapping procedure. Mol Biol Evol 2001; 18:1204–1219.PubMedGoogle Scholar
  90. 90.
    Holland PWH, Garcia-Fernández J, Williams NA et al. Gene duplication and the origins of vertebrate development. Development (Suppl.) 1994:125–133.Google Scholar
  91. 91.
    Kim CB, Amemiya C, Bailey W et al. Hox cluster genomics in the horn shark, Heterodontus francisci. Proc Natl Acad Sci USA 2000; 97:1655–1660.PubMedCrossRefGoogle Scholar
  92. 92.
    Prohaska SJ, Fried C, Amemiya CT et al. The shark HoxN cluster is homologous to the human HoxD cluster. J Mol Evol 2004; 58:212–217.PubMedCrossRefGoogle Scholar
  93. 93.
    Bailey W, Kim J, Wagner G et al. Phylogenetic reconstruction of vertebrate hox cluster duplications. Mol Biol Evol 1997; 14(8):843–853.PubMedGoogle Scholar
  94. 94.
    Aparicio S, Hawker K, Cottage A et al. Organization of the Fugu rubripes Hox clusters: Evidence for continuing evolution of vertebrate Hox complexes. Nat Genetics 1997; 16:79–83.CrossRefGoogle Scholar
  95. 95.
    Prohaska S, Stadler PF. The duplication of the hox gene clusters in teleost fishes. Th Biosci 2004; 123:33–68.CrossRefGoogle Scholar
  96. 96.
    Taylor J, Braasch I, Frickey T et al. Genome duplication, a trait shared by 22,000 species of ray-finned fish. Genome Res 2003; 13:382–390.PubMedCrossRefGoogle Scholar
  97. 97.
    Vandepoele K, De Vos W, Taylor JS et al. Major events in the genome evolution of vertebrates: Paranome age and size differ considerably between ray-finned fishes and land vertebrates. Proc Natl Acad Sci USA 2004; 101:1638–1643.PubMedCrossRefGoogle Scholar
  98. 98.
    Chiu CH, Dewar K, Wagner GP et al. Amemiya. Bichir HoxA cluster sequence reveals surprising trends in rayfinned fish genomic evolution. Genome Res 2004; 14:11–17.PubMedCrossRefGoogle Scholar
  99. 99.
    Metscher BD, Takahashi K, Crow K et al. Expression of hoxa-11 and hoxa-13 in the pectoral fin of a basal ray-finned fish, polyodon spathula: Implications for the origin of tetrapod limbs. Evol Dev 2005; 7:186–195.PubMedCrossRefGoogle Scholar
  100. 100.
    Hoegg S, Brinkmann H, Taylor J et al. Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J Mol Evol 2004; 59(2):190–203.PubMedCrossRefGoogle Scholar
  101. 101.
    Kobel H, Du Pasquier L. Genetics of polyploid xenopus. Trends Genet 1986; 12:310–315.CrossRefGoogle Scholar
  102. 102.
    Courtet M, Flajnik M, Du Pasquier L. Major histocompatibility complex and immunoglobulin loci visualized by in situ hybridization on Xenopus chromosomes. Dev Comp Immunol 2001; 25.Google Scholar
  103. 103.
    Fares MA, Bezemer D, Moya A et al. Selection on coding regions determined Hox7 genes evolution. Mol Biol Evol 2003; 20(12):2104–2112.PubMedCrossRefGoogle Scholar
  104. 104.
    Larhammar D, Risinger C. Molecular genetic aspects of tetraploidy in the common carp Cyprinus carpio. Mol Phylogenet Evol 1994; 3:59–68.PubMedCrossRefGoogle Scholar
  105. 105.
    Levine EM, Schechter N. Homeobox genes expressed in the retina and brain of adult goldfish. Proc Natl Acad Sci USA 1993; 90:2729–2733.PubMedCrossRefGoogle Scholar
  106. 106.
    Ferris SD, Whitt GS. Evolution of the differential regulation of duplicate genes after polyploidization. J Mol Evol 1979; 12:267–317.PubMedCrossRefGoogle Scholar
  107. 107.
    Nadeau JH, Sankoff D. Comparable rates of gene loss and functional divergence after genome duplications early in vertebrate evolution. Genetics 1997; 147:1259–1266.PubMedGoogle Scholar
  108. 108.
    Wendel JF. Genome evolution in polypoids. Plant Mol Biol 2000; 42:225–249.PubMedCrossRefGoogle Scholar
  109. 109.
    Lynch M, Conery JS. The evolutionary fate and consequences of duplicate genes. Science 2000; 290:1151–1155.PubMedCrossRefGoogle Scholar
  110. 110.
    Amores A, Suzuki T, Yan YL et al. Developmental roles of pufferfish Hox clusters and genome evolution in ray-fin fish. Genome Res 2004; 14:1–10.PubMedCrossRefGoogle Scholar
  111. 111.
    Chiu CH, Dewar K, Wagner GP et al. Bichir HoxA cluster sequence reveals surprising trends in ray-finned fish genomic evolution. Genome Res 2004; 14:11–17.PubMedCrossRefGoogle Scholar
  112. 112.
    Mannaert A, Roelants K, Bossuyt F et al. A PCR survey for posterior hox genes in amphibians. Mol Phylogenet Evol 2006; 38:449–458.PubMedCrossRefGoogle Scholar
  113. 113.
    Hoegg S, Meyer A. Hox clusters as models for vertebrate genome evolution. Trends Genet 2005; 21:421–424.PubMedCrossRefGoogle Scholar
  114. 114.
    Luo J, Stadler PF, Meyer A et al. PCR survey of Hox genes in the goldfish. Carassius auratus auratus. 2006, (submitted).Google Scholar
  115. 115.
    Chiu CH, Nonaka D, Xue L et al. Evolution of Hoxa-11 in lineages phylogenetically positioned along the fin-limb transition. Mol Phylogen Evol 2000; 17:305–316.CrossRefGoogle Scholar
  116. 116.
    van de Peer Y, Taylor JS, B I et al. The ghost of selection past: Rates of evolution and functinal divergence of anciently duplicated genes. J Mol Evol 2001; 53:436–446.PubMedCrossRefGoogle Scholar
  117. 117.
    Wagner GP, Takahashi K, Lynch V et al. Molecular evolution of duplicated ray finned fisch hoxa clusters: Increased synonymous substitution rate and asymmetrical codivergence of coding and noncoding sequences. J Mol Evol 2005; 60:665–676.PubMedCrossRefGoogle Scholar
  118. 118.
    Steinke D, Salzburger W, Braasch I et al. Many genes in fish have species-specific asymmetric rates of molecular evolution. BMC Genomics 2006; 7:20, [epub].PubMedCrossRefGoogle Scholar
  119. 119.
    Ludwig MZ, Bergman C, Patel NH et al. Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 2000; 403:564–567.PubMedCrossRefGoogle Scholar
  120. 120.
    Carter AJ, Wagner GP. Evolution of functionally conserved enhancers can be accelerated in large populations: A population-genetic model. Proc R Soc Lond B Biol Sci 2002; 269:953–960.CrossRefGoogle Scholar
  121. 121.
    Tumpel S, Cambronero F, Wiedemann LM et al. Evolution of cis elements in the differential expression of two Hoxa2 coparalogous genes in pufferfish (Takifugu rubripes). Proc Natl Acad Sci USA 2006; 103:5419–5424.PubMedCrossRefGoogle Scholar
  122. 122.
    Wagner G, Fried C, Prohaska S et al. Divergence of conserved noncoding sequences: Rate estimates and relative rate tests. Mol Biol Evol 2004; 21(11):2116–2121.PubMedCrossRefGoogle Scholar
  123. 123.
    Lynch VJ, Roth JJ, Wagner GP. Adaptive evolution of Hox-gene homeodomains after cluster duplication. 2006, (submitted).Google Scholar
  124. 124.
    Force A, Lynch M, Pickett F et al. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 1999; 151(4):1531–1545.PubMedGoogle Scholar
  125. 125.
    Prince V, Pickett FB. Splitting pairs: The diverging fates of duplicated genes. Nat Rev Genet 2002;3.Google Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2007

Authors and Affiliations

  • Sonja J. Prohaska
    • 1
  • Peter F. Stadler
    • 2
  • Günter P. Wagner
    • 3
  1. 1.Department of Computer Science and EngineeringArizona State UniversityPhoenixUSA
  2. 2.Lehrstuhl für Bioinformatik Institut für InformatikUniversität LeipzigLeipzigGermany
  3. 3.Barmhertig Brüder-HospitalWienAustria

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