Evo-devo of non-bilaterian animals

Genetics and Molecular Biology

Volumn 38, Issue 3, 2015, Pages 284-300

  Lanna, Emilio ^a  

^a FEDERAL UNIVERSITY OF BAHIA   (Brazil)

Author keywords

BMP; Early diverging metazoans; Evolution; FGF; Nervous system; Stem cells; Wnt

Indexed keywords

TRANSCRIPTION FACTOR;

ANTERIOR POSTERIOR AXIS; CELL LINEAGE; CNIDARIA; CRISPR CAS SYSTEM; CTENOPHORA; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EMBRYO POLARITY; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; GASTRULATION; GENE EXPRESSION; GERM LAYER; MESODERMAL CELL; MUSCLE TISSUE; NERVOUS TISSUE; NONHUMAN; PHYLOGENY; PLACOZOA; REVIEW; RNA INTERFERENCE; SOMATIC CELL; SPONGE (PORIFERA); STEM CELL; WNT SIGNALING PATHWAY;

EID: 84941626082     PISSN: 14154757     EISSN: 16784685     Source Type: Journal    
DOI: 10.1590/S1415-475738320150005     Document Type: Review

References (139)

1. Adamska M, Degnan SM, Green KM, Adamski M, Craigie A, Larroux C and Degnan BM (2007) Wnt and TGF-expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning. PLoS ONE 2:e1031.
2. Adamska M, Degnan BM, Green K and Zwafink C (2011) What sponges can tell us about the evolution of developmental processes. Zoology 114:1-10.
3. Adell T, Grebenjuk VA, WiensMand Muller WEG (2003) Isolation and characterization of two T-box genes from sponges, the phylogenetically oldest metazoan taxon. Dev Genes Evol 213:421-434.
4. Alié A and Manuel M (2010) The backbone of the post-synaptic density originated in a unicellular ancestor of choanoflagellates and metazoans. BMC Evol Biol 10:e34.
5. Alie A, Leclére L, Jager M, Dayraud C, Chang P, Le Guyader H, Queinnec E and Manuel M (2011) Somatic stem cells express Piwi and Vasa genes in an adult ctenophore: Ancient association of “germline genes” with stemness. Dev Biol 350:183-197.
6. Ambrosone A, Marchesano V, Tino A, Hobmayer B and Tortiglione C (2012) Hymyc1 downregulation promotes stem cell proliferation in Hydra vulgaris. PLoS One 7:e30660.
7. Amiel A and Houliston E (2009) Three distinct RNA localization mechanisms contribute to oocyte polarity establishment in the cnidarian Clytia hemisphærica. Dev Biol 327:191-203.
8. Anderson PA (2015) On the origins of that most transformative of biological systems-the nervous system. J Exp Biol 218:504-505.
9. Araújo H, FonteneleMRand da Fonseca RN (2011) Position matters: Variability in the spatial pattern of BMP modulators generates functional diversity. Genesis 49:698-718.
10. Arendt D (2008) The evolution of cell types in animals: Emerging principles from molecular studies. Nat Rev Genet 9:868-882.
11. Borojevic R (1966) Étude expérimentale de la différenciation des cellules de l’éponge au cours de son développement. Dev Biol 14:130-153.
12. Borojevic R and Levi C (1964) Métamorphose artificielle de larves d’Éponges, aprés dissociation et réagrégation des cellules larvaires. C R Acad Sci Paris 259:4364-4366.
13. Bosch TCG, Anton-Erxleben F, Hemmrich G and Khalturin K (2010) The Hydra polyp: Nothing but an active stem cell community. Dev Growth Differ 52:15-25.
14. Broun M, Gee L, Reinhardt B and Bode HR (2005) Formation of the head organizer in hydra involves the canonical Wnt pathway. Development 132:2907-2916.
15. Browne EN (1909) The production of new hydranths in hydra by the insertion of small grafts. J Exp Zool 7:1-23.
16. Brusca RC and Brusca GJ (2003) Invertebrates. 2nd edition. Sinauer Ass. Inc, Sunderland, 888 pp.
17. Burton PM (2008) Insights from diploblasts; the evolution of mesoderm and muscle. J Exp Zool 310B:5-14.
18. Burton PM and Finnerty JR (2009) Conserved and novel gene expression between regeneration and asexual fission in Nematostella vectensis. Dev Genes Evol 219:79-87.
19. Byrun CA and Martindale MQ (2004) Gastrulation in the Cnidaria and Ctenophora. In: Stern C (ed) Gastrulation: From Cell to Embryo. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 33-49.
20. Carroll SB, Grenier JK and Weatherbee SD (2005) From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design. 2nd edition. Blackwell Publishing, Oxford, 258 pp.
21. Chapman JA, Kirkness EF, Simakov O, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D, et al. (2010) The dynamic genome of Hydra. Nature 464:592-596.
22. Collins AG, Chuchert PS, Marques AC, Jankowski T, Medina M and Schierwater BS (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.
23. Cummings SG and Bode HR (1984) Head regeneration and polarity reversal in Hydra attenuata can occur in the absence of DNA synthesis. Rouxs Arch Dev Biol 194:79-86.
24. Dayraud C, Alie A, Jager M, Chang P, Le Guyader H, Manuel M and Queinnec E (2012) Independent specialisation of myosin II paralogues in muscle vs. non-muscle functions during early animal evolution: A ctenophore perspective. BMC Evol Biol 12:e107.
25. Degnan BM, Vervoort M, Larroux C and Richards G (2009) Early evolution of metazoan transcription factors. Curr Opin Genet Dev 19:591-599.
26. Derelle R and Manuel M (2007) Ancient connection between NKL genes and the mesoderm? Insights from Tlx expression in a ctenophore. Dev Genes Evol 217:253-261.
27. De Robertis EM (2008) Evo-Devo: Variations on ancestral themes. Cell 132:185-195.
28. DohrmannMand Wörheide G (2013) Novel scenarios of early animal evolution -Is it time to rewrite textbooks? Integr Comp Biol 53:503-511.
29. Eckelbarger KJ and Larson R (1992) Ultrastructure of the ovary and oogenesis in the jellyfish Linuche unguiculata and Stomolophus meleagris, with a review of ovarian structure in the Scyphozoa. Mar Biol 114:633-643.
30. Edgecombe GD, Giribet G, Dunn CW, Hejnol A, Kristensen RM, Neves RC, Rouse GW, Worsaae K and Sorensen MV (2011) Higher-level metazoan relationships: Recent progress and remaining questions. Org Divers Evol 11:151-172.
31. Eitel M, Guidi L, Hadrys H, BalsamoMand Schierwater B (2011) New insights into placozoan sexual reproduction and development. PLoS ONE 6:e19639.
32. Ereskovsky AV (2010) The Comparative Embryology of Sponges. Springer, Dordrecht, Heidelberg, London, New York, 329 pp.
33. Ereskovsky AV, Borchiellini C, Gazave E, Ivanisevic J, Lapebie P, Perez T, Renard E and Vacelet J (2009) The Homoscleromorph sponge Oscarella lobularis, a promising sponge model in evolutionary and developmental biology. Bioessays 31:89-97.
34. Ereskovsky AV, Renard E and Borchiellini C (2013) Cellular and molecular processes leading to embryo formation in sponges: Evidences for high conservation of processes throughout animal evolution. Dev Genes Evol 223:5-22.
35. Erwin DH, Laflamme M, Tweedt SM, Sperling EA, Pisani D and Peterson KJ (2011) The Cambrian conundrum: Early divergence and later ecological success in the early history of animals. Science 334:1091-1097.
36. Ewen-Campen B, Schwager EE and Extavour CGM (2010) The molecular machinery of germ line specification. Mol Reprod Dev 77:3-18.
37. Extavour CG and Akam M (2003) Mechanisms of germ cell specification across the metazoans: Epigenesis and preformation. Development 130:5869-5884.
38. Extavour CG, Pang K, Matus DQ and Martindale MQ (2005) vasa and nanos expression patterns in a sea anemone and the evolution of bilaterian germ cell specification mechanisms. Evol Dev 7:201-215.
39. Finnerty JR, Pang K, Burton P, Paulson D and Martindale MQ (2004) Origins of bilateral symmetry: Hox and dpp expression in a sea anemone. Science 304:1335-1337.
40. Fortunato SA, Adamski M, Ramos OM, Leininger S, Liu J, Ferrier DE and Adamska M (2014) Calcisponges have a ParaHox gene and dynamic expression of dispersed NK homeobox genes. Nature 514:620-623.
41. Freeman G (1983) Experimental studies on embryogenesis in hydrozoans (Trachylina and Siphonophora) with direct development. Biol Bull 165:591-618.
42. Fuchs B, Wang W, Graspeuntner S, Li Y, Insua S, Herbst EM, Dirksen P, Böhm A-M, Hemmrich G, Sommer F (2014). Regulation of polyp-to-jellyfish transition in Aurelia aurita. Curr Biol 24:263-273.
43. Funayama N (2010) The stem cell system in demosponges: Insights into the origin of somatic stem cells. Dev Growth Differ 52:1-14.
44. Funayama N (2013) The stem cell system in demosponges: Suggested involvement of two types of cells: Archeocytes (active stem cells) and choanocytes (food-entrapping flagellated cells). Dev Genes Evol 223:23-38.
45. Galliot B, Quiquand M, Ghila L, de Rosa R, Miljkovic-Licina M and Chera S (2009) Origins of neurogenesis, a cnidarian view. Dev Biol 322:2-24.
46. Gilbert S (2010) Developmental Biology. 9th edition, Sinauer Associates, Inc., Sunderland, 711 pp.
47. Giles AF and Averof M (2014) Functional genetics for all: Engineered nucleases, CRISPR and the gene editing revolution. EvoDevo 5:e43.
48. Gold DA and Jacobs DK (2013) Stem cell dynamics in Cnidaria: Are there unifying principles? Dev Genes Evol 223:53-66.
49. Grens A, Mason E, Marsh JL and Bode HR (1995) Evolutionary conservation of a cell fate specification gene: The Hydra achaete-scute homolog has proneural activity in Drosophila. Development 121:4027-4035.
50. Grimson A, Srivastava M, Fahey B, Woodcroft BJ, Chiang HR, King N, Degnan BM, Rokhsar DS and Bartel, DP (2008) Early origins and evolution of microRNAs and Piwiinteracting RNAs in animals. Nature 455:1193-1197.
51. Hadrys T, DeSalle R, Sagasser S, Fischer N and Schierwater B (2005) The Trichoplax PaxB gene: A putative Proto-PaxA/B/C gene predating the origin of nerve and sensory cells. Mol Biol Evol 22:1569-1578.
52. Harbison GR (1985) On the classification and evolution of the Ctenophora. In: Conway Morris S, George JD, Gibson R and Platt HM (eds) The Origins and Relationships of Lower Invertebrates. Clarendon, Oxford, 400 pp.
53. Hemmrich G and Bosch TC (2008) Compagen, a comparative genomics platform for early branching metazoan animals, reveals early origins of genes regulating stem-cell differentiation. Bioessays 30:1010-1018.
54. Holland PWH (2013) Evolution of homeobox genes. WIREs Dev Biol 2:31-45.
55. Houliston E, Momose T and Manuel M (2010) Clytia hemisphaerica: A jellyfish cousin joins the laboratory. Trends Genet 26:159-167.
56. Jager M, Chiori R, Alié A, Dayraud C, Quéinnec E and Manuel M (2011) New insights on ctenophore neural anatomy: Immunofluorescence study in Pleurobrachia pileus (Müller, 1776). J Exp Zool B Mol Dev Evol 316:171-187.
57. Jager M, Dayraud C, Mialot A, Quéinnec E, Le Guyader H and Manuel M (2013) Evidence for involvement of Wnt signalling in body polarities, cell proliferation, and the neurosensory system in an adult ctenophore. PLoS ONE 8:e84363.
58. Jakob W, Sagasser S, Dellaporta S, Holland P, Kuhn K and Schierwater B (2004) The Trox-2 Hox/ParaHox gene of Trichoplax (Placozoa) marks an epithelial boundary. Dev Genes Evol 214:170-175.
59. Jenner RA and Wills MA (2007) The choice of model organisms in evo-devo. Nat Rev Genet 8:311-319.
60. Koizumi, O (2006) Nerve ring of the hypostome in Hydra: Is it an origin of the central nervous system of bilaterian animals? Brain Behav Evol 69:151-159.
61. Kraus Y, Fritzenwanker JH, Genikhovich G and Technau U (2007) The blastoporal organiser of a sea anemone. Curr Biol 17:R874-R876.
62. Kraus Y, Flici H, Hensel K, Plickert G, Leitz T and Frank U (2014) The embryonic development of the cnidarian Hydractinia echinata. Evol Dev 16:323-338.
63. Kunzel T, Heiermann R, Frank U, Muller W, Tilmann W, Bause M, Nonn A, Helling M, Schwarz RS and Plickert G (2010). Migration and differentiation potential of stem cells in the cnidarian Hydractinia analysed in eGFP-transgenic animals and chimeras. Dev Biol 348:120-129.
64. Lanna E and Klautau M (2010) Oogenesis and spermatogenesis in Paraleucilla magna (Porifera, Calcarea). Zoomorphology 129:249-261.
65. Lapébie P, Gazave E, Ereskovsky A, Derelle R, Bézac C, Renard E, Houliston E and Borchiellini C (2009) WNT/_-Catenin signalling and epithelial patterning in the homoscleromorph sponge Oscarella. PLoS ONE 4:e5823.
66. Larroux C, Fahey B, Degnan SM, Adamski M, Rokhsar DS and Degnan BM (2007) The NK homeobox gene cluster predates the origin of Hox genes. Curr Biol17:706-710.
67. Leclère L, Jager M, Barreau C, Chang P, Le Guyader H, Manuel M and Houliston E (2012) Maternally localized germ plasm mRNAs and germ cell/stem cell formation in the cnidarian Clytia. Dev Biol 364:236-248.
68. Leclère L and Rentzsch F (2014) RGM regulates BMP-mediated secondary axis formation in the sea anemone Nematostella vectensis. Cell Rep 9:1921-1930.
69. Lee PN, Pang K, Matus DQ and Martindale MQ (2006) AWNTof things to come: Evolution of Wnt signaling and polarity in cnidarians. Semin Cell Dev Biol 17:157-167.
70. Leininger S, Adamski M, Bergum B, Guder C, Liu J, Laplante M, Bråte J, Hoffmann F, Fortunato S, Jordal S, et al. (2014) Developmental gene expression provides clues to relationships between sponge and eumetazoan body plans. Nat Commun 5:e3905.
71. Leys SP (2004) Gastrulation in sponges. In: Stern C (ed) Gastrulation: From Cell to Embryo. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 23-31.
72. Leys SP (2015) Elements of a ‘nervous system’ in sponges. J Exp Biol 218:581-591.
73. Leys SP and Hill A (2012) The physiology and molecular biology of sponge tissues. Adv Mar Biol 62:1-56.
74. Maldonado M and Bergquist PR (2002) Porifera. In: Young CM, Sewell MA and Rice ME (eds) Atlas of Marine Invertebrate Larvae. Academic Press, San Diego, pp. 21-50.
75. Maldonado M and Riesgo A (2008) Reproduction in Porifera: A synoptic overview. Treb Soc Catalana Biol 59:29-49.
76. Manuel M (2009) Early evolution of symmetry and polarity in metazoan body plans. C R Biol 332:184-209.
77. Marlow H, Matus DQ and Martindale MQ (2013) Ectopic activation of the canonical wnt signaling pathway affects ectodermal patterning along the primary axis during larval development in the anthozoan Nematostella vectensis. Dev Biol 380:324-334.
78. Martindale MQ (2005) The evolution of metazoan axial properties. Nat Rev Genet 6:917-927.
79. Martindale MQ and Henry JQ (1996) Development and regeneration of comb plates in the ctenophore Mnemiopsis leidyi. Biol Bull 191:290-292.
80. MartindaleMQand Henry JQ (1997) Ctenophorans, the comb jellies. In: Gilbert S and Raunio AM (eds) Embryology: Constructing the Organism. Sinauer, Sunderland, pp. 87-111.
81. Martindale MQ, Pang K and Finnerty JR (2004) Investigating the origins of triploblasty: ‘Mesodermal’ gene expression in a diploblastic animal, the sea anemone, Nematostella vectensis (phylum, Cnidaria; Class Anthozoa). Development 131:2463-2474.
82. Mendivil Ramos OM, Barker D and Ferrier DE (2012) Ghost loci imply Hox and ParaHox existence in the last common ancestor of animals. Curr Biol 22:1951-1956.
83. Momose T, Derelle R and Houliston E (2008) A maternally localised Wnt ligand required for axial patterning in the cnidarian Clytia hemisphaerica. Development 135:2105-2113.
84. Monteiro AS, Schierwater B, Dellaporta SL and Holland PWH (2006) A low diversity of ANTP class homeobox genes in Placozoa. Evol Dev 8:174-182.
85. Moroz LL (2009) On the independent origins of complex brains and neurons. Brain Behav Evol 74:177.
86. Moroz LL, Kocot KM, Citarella MR, Dosung S, Norekian TP, Povolotskaya IS, Grigorenko AP, Dailey C, Berezikov E, Buckley KM, et al. (2014) The ctenophore genome and the evolutionary origins of neural systems. Nature 510:109-116.
87. Nakanishi N, Sogabe S and Degnan B (2014) Evolutionary origin of gastrulation: Insights from sponge development. BMC Biol 12:e26.
88. Nichols SA, Dirks W, Pearse JS and King N (2006) Early evolution of animal cell signaling and adhesion genes. Proc Natl Acad Sci USA 103:12451-12456.
89. Nielsen C (2008) Six major steps in animal evolution: Are we derived sponge larvae? Evol Dev 10:241-257.
90. Okamoto K, Nakatsukasa M, Alie A, Masuda Y, Agata K and Funayama N (2012) The active stem cell specific expression of sponge Musashi homolog EflMsiA suggests its involvement in maintaining the stem cell state. Mech Dev 129:24-37.
91. Pang K, Ryan JF, NISC Comparative Sequencing Program, Mullikin JC, Baxevanis AD and Martindale MQ (2010) Genomic insights into Wnt signaling in an early diverging metazoan, the ctenophore Mnemiopsis leidyi. EvoDevo 1:e10.
92. Pang K, Ryan JF, Baxevanis AD and Martindale MQ (2011) Evolution of the TGF-b signaling pathway and its potential role in the ctenophore, Mnemiopsis leidyi. PLoS ONE 6:e24152.
93. Perovic-Ottstadt S, Cetkovic H, Gamulin V, Schröder HC, Kropf K, Moss C, Korzhev M, Diehl-Seifert B, Müller IM and Müller WEG (2004) Molecular markers for germ cell differentiation in the demosponge Suberites domuncula. Int J Dev Biol 48:293-305.
94. Petersen CP and Reddien PW (2009) Wnt signaling and the polarity of the primary body axis. Cell 139:1056-1068.
95. Philippe H, Derelle R, Lopez P, Pick K, Borchiellini C, Boury-Esnault N, Vacelet J, Renard E, Houliston E, Queinnec E, et al. (2009) Phylogenomics revives traditional views on deep animal relationships. Curr Biol 19:706-712.
96. Philippe H, Brinkmann H, Lavrov DV, Littlewood DTJ, Manuel M, Wörheide G and Baurain D (2011) Resolving difficult phylogenetic questions: Why more sequences are not enough. PLoS Biol 9:e1000602.
97. Piatgorsky J and Kozmik Z (2004). Cubozoan jellyfish: An Evo/Devo model for eyes and other sensory systems. Int J Dev Biol 48:719-729.
98. Plickert G, Jacoby V, Frank U, Müller WA and Mokady O (2006) Wnt signaling in hydroid development: Formation of the primary body axis in embryogenesis and its subsequent patterning. Dev Biol 298:368-378.
99. Plickert G, Frank U and Müller WA (2012) Hydractinia, a pioneering model for stem cell biology and reprogramming somatic cells to pluripotency. Int J Dev Biol 56:519-534.
100. Podar M, Haddock SHD, Sogin ML and Harbison GR (2001) A molecular phylogenetic framework for the phylum Ctenophora using 18S rRNA genes. Mol Phylogenet Evol 21:218-230.
101. Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV, et al. (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86-94.
102. Renfer E, Amon-Hassenzahl A, Steinmetz PR and Technau U (2010) A muscle-specific transgenic reporter line of the sea anemone, Nematostella vectensis. Proc Natl Acad Sci USA 107:104-108.
103. Rentzsch F, Guder C, Vocke D, Hobmayer B and Holstein TW (2007) An ancient chordin-like gene in organizer formation of Hydra. Proc Natl Acad Sci 104:3249-3254.
104. Rentzsch F, Fritzenwanker JH, Scholz CB and Technau U (2008) FGF signalling controls formation of the apical sensory organ in the cnidarian Nematostella vectensis. Development 135:1761-1769.
105. Richards GS, Simionato E, Perron M, Adamska M, Vervoort M and Degnan BM (2008) Sponge genes provide new insight into the evolutionary origin of the neurogenic circuit. Curr Biol 18:1156-1161.
106. Riesgo A, Farrar N, Windsor PJ, Giribet G and Leys SP (2014) The analysis of eight transcriptomes from all poriferan classes reveals surprising genetic complexity in sponges. Mol Biol Evol 31:1102-1120.
107. Rivera AS, Hammel JU, Haen KM, Danka ES, Cieniewicz B, Winters IP, Posfai D, Wörheide G, Lavrov D, Knight SW, et al. (2011) RNA interference in marine and freshwater sponges: Actin knockdown in Tethya wilhelma and Ephydatia muelleri by ingested dsRNA expressing bacteria. BMC Bioltechnol 11:e67.
108. Ryan JF (2014) Did the ctenophore nervous system evolve independently? Zoology 117:225-226.
109. Ryan JF and Baxevanis AD (2007) Hox, Wnt, and the evolution of the primary body axis: Insights from the early-divergent phyla. Biol Direct 13:e37.
110. Ryan JF, Burton PM, Mazza ME, Kwong GK, Mullikin JC and Finnerty JR (2006) The cnidarian-bilaterian ancestor possessed at least 56 homeoboxes: Evidence from the starlet sea anemone, Nematostella vectensis. Genome Biol:R64.
111. Ryan JF, Pang K, NISC Comparative Sequencing Program, Mullikin JC, Martindale MQ and Baxevanis AD (2010) The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa. EvoDevo 1:e9.
112. Ryan JF, Pang K, Schnitzler CE, Nguyen A-D, Moreland RT, Simmons DK, Koch BJ, Francis WR, Havlak P, Smith SA, et al. (2013) The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342:1242592-1-1242592-8.
113. Saina M, Genikhovich G, Renfer E and Technau U (2009) BMPs and chordin regulate patterning of the directive axis in a sea anemone. Proc Natl Acad Sci 106:18592-18597.
114. Schierwater B, de Jong D and DeSalle R (2009) Placozoa and the evolution of Metazoa and intrasomatic cell differentiation. Int J Biochem Cell Biol 41:370-379.
115. Seipel K and Schmid V (2006) Mesodermal anatomies in cnidarian polyps and medusae. Int J Dev Biol 50:589-599.
116. Seipel K, Yanze N and Schmid V (2004) Developmental and evolutionary aspects of the basic helix-loop-helix transcription factors Atonal-like 1 and Achaete-scute homolog 2 in the jellyfish. Dev Biol 269:331-345.
117. Sinigaglia C, Busengdal H, Lerner A, Oliveri P and Rentzsch F (2015) Molecular characterization of the apical organ of the anthozoan Nematostella vectensis. Dev Biol 398:120-133.
118. Shinzato C, Shoguchi E, Kawashima T, Hamada M, Hisata K, Tanaka M, Fujie M, Fujiwara M, Koyanagi R, Ikuta T, et al. (2011) Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476:320-324.
119. Simion P, Bekkouche N, Jager M, Quéinnec E, Manuel M (2015) Exploring the potential of small RNA subunit and ITS sequences for resolving phylogenetic relationships within the phylum Ctenophora. Zoology 118:102-114.
120. Simmons DK, Pang K and Martindale MQ (2012) Lim homeobox genes in the ctenophore Mnemiopsis leidyi: The evolution of neural cell type specification. EvoDevo 3:e2.
121. Smith CL, Varoqueaux F, Kittelmann M, Azzam RN, Cooper B, Winters CA, Eitel M, Fasshauer D and Reese TS (2014) Novel cell types, neurosecretory cells, and body plan of the early-diverging metazoan Trichoplax adhaerens. Curr Biol 24:1565-1572.
122. Sommer RJ (2009) The future of evo-devo: Model systems and evolutionary theory. Nat Rev Genet 10:416-422.
123. Spemann H and Mangold H (1924) Über Induktion von Embryonalanlagen durch Implantation artfremder Organisatoren.W Roux’s Arch Entwickl-Mech Org. Dev Genes Evol 100:599-638.
124. Spring J, Yanze N, Josch C, Middel AM, Winninger B and Schmid V (2002) Conservation of Brachyury, Mef2, and Snail in the myogenic lineage of jellyfish: A connection to the mesoderm of bilateria. Dev Biol 244:372-384.
125. Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, Kuo A, Mitros T, Salamov A, Carpenter ML, et al. (2008) The Trichoplax genome and the nature of placozoans. Nature 454:955-960.
126. Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier MEA, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, et al. (2010a) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720-726.
127. Srivastava M, Larroux C, Lu DR, Mohanty K, Chapman J, Degnan BM and Rokhsar DS (2010b) Early evolution of the LIM homeobox gene family. BMC Biol 8:e4.
128. Steele RE (2005) Genomics of basal metazoans. Integr Comp Biol 45:639-648.
129. Steinmetz PRH, Kraus JEM, Larroux C, Hammel JU, Amon-Hassenzahl A, Houliston E, Worheide G, Nickel M, Degnan BM and Technau U (2012). Independent evolution of striated muscles in cnidarians and bilaterians. Nature 487:231-234.
130. Technau U and Bode HR (1999) HyBra1, a Brachyury homologue, acts during head formation in Hydra. Development 126:999-1010.
131. Technau U and Scholz CB (2003) Origin and evolution of endoderm and mesoderm. Int J Dev Biol 47:531-539.
132. Technau U and Steele RE (2012) Evolutionary crossroads in developmental biology: Cnidaria. Development 139:1447-1458.
133. Voigt O, Collins AG, Pearse VB, Pearse JS, Ender A, Hadrys H and Schierwater B (2004) Placozoa -no longer a phylum of one. Curr Biol 14:R944-R945.
134. Watanabe H, Fujisawa T and Holstein TW (2009) Cnidarians and the evolutionary origin of the nervous system. Dev Growth Differ 51:167-183.
135. Wiens M, Belikov SI, Kaluzhnaya OV, Adella T, Schroder HC, Perovic-Ottstadt S, Kaandorp JA and Muller WEG (2008) Regional and modular expression of morphogenetic factors in the demosponge Lubomirskia baicalensis. Micron 39:447-460.
136. Wilson HV (1907) On some phenomena of coalescence and regeneration in sponges. J Exp Zool 5:245-258.
137. Windsor PJ and Leys SP (2010) Wnt signaling and induction in the sponge aquiferous system: Evidence for an ancient origin of the organizer. Evol Dev 12:484-493.
138. Wittlieb J, Khalturin K, Lohmann JU, Anton-Erxleben F and Bosch TC (2006) Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis. Proc Natl Acad Sci USA 103:6208-6211.
139. Wörheide G, Dohrmann M, Erpenbeck D, Larroux C, Maldonado M, Voigt O, Borchiellini C and Lavrov DV (2012) Deep phylogeny and evolution of sponges (Phylum Porifera). Adv Mar Biol 61:1-78.