Punctuated emergences of genetic and phenotypic innovations in eumetazoan, bilaterian, euteleostome, and hominidae ancestors

Genome Biology and Evolution

Volumn 5, Issue 10, 2013, Pages 1949-1968

  Wenger, Yvan ^a   Galliot, Brigitte ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Eumetazoan innovations; Gene ontology enrichment; Macroevolution of human orthologs; Orthologomes; Reciprocal best hits (RBHs); Regulatory based parallel evolution

Indexed keywords

PROTEIN; PROTEOME;

ANIMAL; ARTICLE; CLASSIFICATION; CNIDARIA; EUMETAZOAN INNOVATIONS; GENE ONTOLOGY ENRICHMENT; GENETICS; GENOMICS; HOMINID; HUMAN; MACROEVOLUTION OF HUMAN ORTHOLOGS; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; ORTHOLOGOMES; PHYLOGENY; RECIPROCAL BEST HITS (RBHS); REGULATORY-BASED PARALLEL EVOLUTION;

EUMETAZOAN INNOVATIONS; GENE ONTOLOGY ENRICHMENT; MACROEVOLUTION OF HUMAN ORTHOLOGS; ORTHOLOGOMES; RECIPROCAL BEST HITS (RBHS); REGULATORY-BASED PARALLEL EVOLUTION;

ANIMALS; CNIDARIA; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENOMICS; HOMINIDAE; HUMANS; PHYLOGENY; PROTEINS; PROTEOME;

EID: 84892505668     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evt142     Document Type: Article

References (103)

1. Aboobaker AA, BlaxterML 2003. Hox gene loss during dynamic evolution of the nematode cluster. Curr Biol. 13:37-40.
2. Adams MD, et al. 2000. The genome sequence of Drosophila melanogaster. Science 287:2185-2195.
3. Adoutte A, Balavoine G, Lartillot N, de Rosa R. 1999. Animal evolution The end of the intermediate taxa?. Trends Genet. 15:104-108.
4. Alie A, Manuel M. 2010. The backbone of the post-synaptic density originated in a unicellular ancestor of choanoflagellates and metazoans. BMC Evol Biol. 10:34.
5. Altenhoff AM, Dessimoz C. 2012. Inferring orthology and paralogy. Methods Mol Biol. 855:259-279.
6. Arendt D. 2008. The evolution of cell types in animals: emerging principles from molecular studies. Nat Rev Genet. 9:868-882.
7. Ashburner M, et al. 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 25:25-29.
8. Ayala FJ, Rzhetsky A, Ayala FJ. 1998. Origin of the metazoan phyla: molecular clocks confirm paleontological estimates. Proc Natl Acad Sci U S A. 95:606-611.
9. Ball EE, Hayward DC, Saint R, Miller DJ. 2004. A simple plan-cnidarians and the origins of developmental mechanisms. Nat Rev Genet. 5: 567-577.
10. Battacharya D, Yoon HS, Hedges SB, Hackett JD. 2009. Eukaryotes (eukaryota). In: Hedges SB, Kumar S, editors. The timetree of life. Oxford: Oxford University Press. p. 116-120.
11. Blake JA, Grassle JP, Eckelbarger KJ. 2009. Capitella teleta, a new species designation for the opportunistic and experimental Capitella sp. I, with a review of the literature for confirmed records. Zoosymposia 2:25-53.
12. Boyle EI, et al. 2004. Go::Termfinder-open source software for accessing gene ontology information and finding significantly enriched gene ontology terms associated with a list of genes. Bioinformatics 20: 3710-3715.
13. Bridgham JT, et al. 2010. Protein evolution by molecular tinkering: Diversification of the nuclear receptor superfamily from a liganddependent ancestor. PLoS Biol. 8:e1000497.
14. Carroll SB. 2008. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134:25-36.
15. Chapman JA, et al. 2010. The dynamic genome of Hydra. Nature 464: 592-596.
16. Chen F, Mackey AJ, Vermunt JK, Roos DS. 2007. Assessing performance of orthology detection strategies applied to eukaryotic genomes. PLoS One 2:e383.
17. Chervitz SA, et al. 1998. Comparison of the complete protein sets of worm and yeast: orthology and divergence. Science 282:2022-2028.
18. Chisholm AD, Horvitz HR. 1995. Patterning of the Caenorhabditis elegans head region by the pax-6 family member vab-3. Nature 377:52-55.
19. Ciliberti S, Martin OC, Wagner A. 2007. Innovation and robustness in complex regulatory gene networks. Proc Natl Acad Sci U S A. 104: 13591-13596.
20. Cliften PF, Fulton RS,Wilson RK, Johnston M. 2006. After the duplication: gene loss and adaptation in saccharomyces genomes. Genetics 172: 863-872.
21. Collins AG, et al. 2006. Medusozoan phylogeny and character evolution clarified by new large and small subunit rdna data and an assessment of the utility of phylogenetic mixture models. Syst Biol. 55:97-115.
22. Conant GC, Wolfe KH. 2008. Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet. 9:938-950.
23. Dayel MJ, et al. 2011. Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta. Dev Biol. 357: 73-82.
24. Dehal P, et al. 2002. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157-2167.
25. Delsuc F, Brinkmann H, Chourrout D, Philippe H. 2006. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965-968.
26. Domazet-Loso T, Brajkovic J, Tautz D. 2007. A phylostratigraphy approach to uncover the genomic history of major adaptations in metazoan lineages. Trends Genet. 23:533-539.
27. Domazet-Loso T, Tautz D. 2010. Phylostratigraphic tracking of cancer genes suggests a link to the emergence of multicellularity in metazoa. BMC Biol. 8:66.
28. Edgar RC. 2010. Search and clustering orders of magnitude faster than blast. Bioinformatics 26:2460-2461.
29. Eichinger L, Pachebat JA, Glockner G, et al. 2005. The genome of the social amoeba Dictyostelium discoideum. Nature 435:43-57.
30. Eichler EE. 2001. Recent duplication, domain accretion and the dynamic mutation of the human genome. Trends Genet. 17:661-669.
31. Foret S, et al. 2010. New tricks with old genes: the genetic bases of novel cnidarian traits. Trends Genet. 26:154-158.
32. Gabaldon T, Koonin EV. 2013. Functional and evolutionary implications of gene orthology. Nat Rev Genet. 14:360-366.
33. Galliot B, Quiquand M. 2011. A two-step process in the emergence of neurogenesis. Eur J Neurosci. 34:847-862.
34. Galliot B, et al. 2009. Origins of neurogenesis, a cnidarian view. Dev Biol. 332:2-24.
35. Gerhart J, Lowe C, Kirschner M. 2005. Hemichordates and the origin of chordates. Curr Opin Genet Dev. 15:461-467.
36. Giaever G, et al. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387-391.
37. Gibbs RA, et al. 2007. Evolutionary and biomedical insights from the rhesus macaque genome. Science 316:222-234.
38. Gompel N, Prud'homme B. 2009. The causes of repeated genetic evolution. Dev Biol. 332:36-47.
39. Gould SJ. 1992. Ontogeny and phylogeny-revisited and reunited. BioEssays 14:275-279.
40. Gould SJ. 2002. The structure of evolutionary theory. Cambridge, MA: Bellknap Press of Harvard University Press.
41. Graziussi DF, Suga H, Schmid V, Gehring WJ. 2012. The "eyes absent" (eya) gene in the eye-bearing hydrozoan jellyfish cladonema radiatum: conservation of the retinal determination network. J Exp Zool B Mol Dev Evol. 318:257-267.
42. Groenen MA, et al. 2000. A consensus linkage map of the chicken genome. Genome Res. 10:137-147.
43. Grosberg RK, Strathmann RR. 2007. The evolution of multicellularity: a minor major transition. Annu Rev Ecol Evol Syst. 38:621-654.
44. Hejnol A, et al. 2009. Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc Biol Sci. 276:4261-4270.
45. Hellsten U, et al. 2010. The genome of the western clawed frog Xenopus tropicalis. Science 328:633-636.
46. Howe K, et al. 2013. The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498-503.
47. Huerta-Cepas J, Dopazo H, Dopazo J, Gabaldon T. 2007. The human phylome. Genome Biol. 8:R109.
48. Initiative TAG. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796-815.
49. Kaessmann H. 2010. Origins, evolution, and phenotypic impact of new genes. Genome Res. 20:1313-1326.
50. Kass-Simon G, Pierobon P. 2007. Cnidarian chemical neurotransmission, an updated overview. Comp Biochem Physiol A Mol Integr Physiol. 146:9-25.
51. King N, Hittinger CT, Carroll SB. 2003. Evolution of key cell signaling and adhesion protein families predates animal origins. Science 301: 361-363.
52. King N, et al. 2008. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451:783-788.
53. Kostrouch Z, et al. 1998. Retinoic acid X receptor in the diploblast, Tripedalia cystophora. Proc Natl Acad Sci U S A. 95:13442-13447.
54. Kozmik Z, et al. 2003. Role of pax genes in eye evolution: a cnidarian paxb gene uniting pax2 and pax6 functions. Dev Cell. 5:773-785.
55. Kusserow A, et al. 2005. Unexpected complexity of the wnt gene family in a sea anemone. Nature 433:156-160.
56. Lander ES, et al. 2001. Initial sequencing and analysis of the human genome. Nature 409:860-921.
57. Louis A, Roest Crollius H, Robinson-Rechavi M. 2012. How much does the amphioxus genome represent the ancestor of chordates? Brief Funct Genomics. 11:89-95.
58. Lowe CB, et al. 2011. Three periods of regulatory innovation during vertebrate evolution. Science 333:1019-1024.
59. Lowe CJ. 2008. Molecular genetic insights into deuterostome evolution from the direct-developing hemichordate Saccoglossus kowalevskii. Philos Trans R Soc Lond B Biol Sci. 363:1569-1578.
60. Marlow HQ, Srivastava M, Matus DQ, Rokhsar D, Martindale MQ. 2009. Anatomy and development of the nervous system of Nematostella vectensis, an anthozoan cnidarian. Dev Neurobiol. 69:235-254.
61. Matus DQ, Pang K, DalyM,Martindale MQ. 2007. Expression of pax gene family members in the anthozoan cnidarian, Nematostella vectensis. Evol Dev. 9:25-38.
62. McLysaght A, Hokamp K, Wolfe KH. 2002. Extensive genomic duplication during early chordate evolution. Nat Genet. 31:200-204.
63. Mitreva M, et al. 2011. The draft genome of the parasitic nematode Trichinella spiralis. Nat Genet. 43:228-235.
64. Moreno-Hagelsieb G, Latimer K. 2008. Choosing blast options for better detection of orthologs as reciprocal best hits. Bioinformatics 24: 319-324.
65. Niimura Y. 2009. On the origin and evolution of vertebrate olfactory receptor genes: comparative genome analysis among 23 chordate species. Genome Biol Evol. 1:34-44.
66. Nilsson DE. 2004. Eye evolution: a question of genetic promiscuity. Curr Opin Neurobiol. 14:407-414.
67. Ohno S. 1999. Gene duplication and the uniqueness of vertebrate genomes circa 1970-1999. Semin Cell Dev Biol. 10:517-522.
68. Ostlund G, et al. 2010. Inparanoid 7: new algorithms and tools for eukaryotic orthology analysis. Nucleic Acids Res. 38:D196-D203.
69. Overbeek R, Fonstein M, D'Souza M, Pusch GD, Maltsev N. 1999. The use of gene clusters to infer functional coupling. Proc Natl Acad Sci U S A. 96:2896-2901.
70. Page RDM, Holmes EC. 1998. Molecular evolution: a phylogenetic approach. Oxford: Blackwell Science Ltd.
71. Pani AM, et al. 2012. Ancient deuterostome origins of vertebrate brain signalling centres. Nature 483:289-294.
72. Peterson KJ, Cotton JA, Gehling JG, Pisani D. 2008. The ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records. Philos Trans R Soc Lond B Biol Sci. 363:1435-1443.
73. Philippe H, et al. 2009. Phylogenomics revives traditional views on deep animal relationships. Curr Biol. 19:706-712.
74. Piatigorsky J, Kozmik Z. 2004. Cubozoan jellyfish: an evo/devo model for eyes and other sensory systems. Int J Dev Biol. 48:719-729.
75. Pineda D, et al. 2002. The genetic network of prototypic planarian eye regeneration is pax6 independent. Development 129:1423-1434.
76. Plachetzki DC, Fong CR, Oakley TH. 2012. Cnidocyte discharge is regulated by light and opsin-mediated phototransduction. BMC Biol. 10:17.
77. Putnam NH, et al. 2008. The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064-1071.
78. Putnam NH, et al. 2007. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86-94.
79. Ratcliff WC, Denison RF, Borrello M, Travisano M. 2012. Experimental evolution ofmulticellularity. Proc Natl Acad Sci U S A. 109:1595-1600.
80. Richards GS, Simionato E, et al. 2008. Sponge genes provide new insight into the evolutionary origin of the neurogenic circuit. Curr Biol. 18: 1156-1161.
81. Richards S, Gibbs RA, et al. 2008. The genome of the model beetle and pest Tribolium castaneum. Nature 452:949-955.
82. Rodriguez RM, Lopez-Vazquez A, Lopez-Larrea C. 2012. Immune systems evolution. Adv Exp Med Biol. 739:237-251.
83. Ruiz-Trillo I, Roger AJ, Burger G, Gray MW, Lang BF. 2008. A phylogenomic investigation into the origin of metazoa. Mol Biol Evol. 25: 664-672.
84. Saina M, Genikhovich G, Renfer E, Technau U. 2009. Bmps and chordin regulate patterning of the directive axis in a sea anemone. Proc Natl Acad Sci U S A. 106:18592-18597.
85. Sakarya O, et al. 2007. A post-synaptic scaffold at the origin of the animal kingdom. PLoS One 2:e506.
86. Savard J, Tautz D, LercherMJ. 2006. Genome-wide acceleration of protein evolution in flies (Diptera). BMC Evol Biol. 6:7.
87. Seipel K, Schmid V. 2006. Mesodermal anatomies in cnidarian polyps and medusae. Int J Dev Biol. 50:589-599.
88. Shinzato C, et al. 2011. Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476:320-323.
89. Shubin N, Tabin C, Carroll S. 2009. Deep homology and the origins of evolutionary novelty. Nature 457:818-823.
90. Srivastava M, et al. 2010. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720-726.
91. Steinmetz PR, et al. 2012. Independent evolution of striated muscles in cnidarians and bilaterians. Nature 487:231-234.
92. Steiper ME, Young NM. 2009. Primates. In: Hedges SB, Kumar S, editors. The timetree of life. Oxford: Oxford University Press. p. 482-486.
93. Stierwald M, Yanze N, Bamert RP, Kammermeier L, Schmid V. 2004. The sine oculis/six class family of homeobox genes in jellyfish with and without eyes: development and eye regeneration. Dev Biol. 274: 70-81.
94. Suga H, et al. 2013. The Capsaspora genome reveals a complex unicellular prehistory of animals. Nat Commun. 4:2325.
95. Suga H, Schmid V, GehringWJ. 2008. Evolution and functional diversity of jellyfish opsins. Curr Biol. 18:51-55.
96. Suga H, et al. 2010. Flexibly deployed pax genes in eye development at the early evolution of animals demonstrated by studies on a hydrozoan jellyfish. Proc Natl Acad Sci U S A. 107:14263-14268.
97. Swalla BJ, Smith AB. 2008. Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives. Philos Trans R Soc Lond B Biol Sci. 363:1557-1568.
98. Technau U, Steele RE. 2011. Evolutionary crossroads in developmental biology: cnidaria. Development 138:1447-1458.
99. Thomas JH. 2008. Genome evolution in Caenorhabditis. Brief Funct Genomic Proteomic. 7:211-216.
100. Venter JC, et al. 2001. The sequence of the human genome. Science 291: 1304-1351.
101. Wenger Y, Galliot B. 2013. RNAseq versus genome-predicted transcriptomes: a large population of novel transcripts identified in an illumina-454 Hydra transcriptome. BMC Genomics 14:204.
102. Wolf YI, Koonin EV. 2012. A tight link between orthologs and bidirectional best hits in bacterial and archaeal genomes. Genome Biol Evol. 4: 1286-1294.
103. Zhang Y, Emmons SW. 1995. Specification of sense-organ identity by a Caenorhabditis elegans pax-6 homologue. Nature 377:55-59.