Advertisement

Origin of Metazoan Developmental Toolkits and Their Expression in the Fossil Record

  • Sarah M. TweedtEmail author
  • Douglas H. Erwin
Chapter
Part of the Advances in Marine Genomics book series (AMGE, volume 2)

Abstract

Developmental regulatory genes (largely transcription factors and signaling pathways) were once viewed as tightly connected to the origin of the morphological features with which they are associated in bilaterians. With the increased study of basal metazoans (sponges and cnidarians) as well as other eukaryotic clades, it is now clear that many of these highly conserved genes arose much earlier in evolution, and served different biological purposes. This provides a new view of the nature of developmental toolkits associated with the early origin of Metazoa: ancient regulatory genes were only later co-opted for the various developmental roles associated with bilaterian morphology. Here we review the nature of the toolkits at the origin of Metazoa, the Placozoan-Eumetazoan last common ancestor (LCA), the Cnidarian-Bilaterian LCA, and the Protostome-Deuterostome LCA. Integrating this data with recent molecular clock results and data on the fossil record reveals long macroevolutionary lags between the origin of the molecular toolkits and their developmental potential, and the origin of crown group morphologies as documented in the fossil record.

Keywords

Metazoa Phylogeny Fossil record Genetic toolkit Ediacaran Cambrian Macroevolution 

Notes

Acknowledgment

SMT and DHE acknowledge financial support from a NASA Astrobiology Institute grant (MIT node; to DHE).

References

  1. Adamska M, Degnan SM, Green KM, Adamski M, Craigie A, Larroux C, Degnan BM (2007) Wnt and TGF-beta expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning. PLoS One 2(10):e1031Google Scholar
  2. Adamska M, Larroux C, Adamski M, Green K, Lovas E, Koop D, Richards GS, Zwafink C, Degnan BM (2010) Structure and expression of conserved Wnt pathway components in the demosponge Amphimedon queenslandica. Evol Dev 12(5):494–518Google Scholar
  3. Adamska M, Degnan BM, Green K, Zwafink C (2011) What sponges can tell us about the evolution of developmental processes. Zoology 114(1):1–10Google Scholar
  4. Aguinaldo AMA, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489–493Google Scholar
  5. Arendt D (2008) The evolution of cell types in animals: emerging principles from molecular studies. Nat Rev Genet 9:868–883Google Scholar
  6. Arendt D, Nubler-Jung K (1994) Inversion of dorso-ventral axis. Nature 371:26Google Scholar
  7. Arendt D, Wittbrodt J (2001) Reconstructing the eyes of Urbilateria. Proc R Soc Lond B Biol Sci 356:1545–1563Google Scholar
  8. Backfisch B, Rajan VBV, Fischer RM, Lohs C, Arboleda E, Tessmar-Raible K, Raible F (2013) Stable transgenesis in the marine annelid Platynereis dumerilii sheds new light on photoreceptor evolution. Proc Natl Acad Sci U S A 110(1):193–198Google Scholar
  9. Baguñà J, Ruiz-Trillo I, Paps J, Loukota M, Ribera C, Jondelius U, Riutort M (2001) The first bilaterian organisms: simple or complex? New molecular evidence. Int J Dev Biol 45(S1):S133–S134Google Scholar
  10. Baguñà J, Martinez P, Paps J, Riutort M (2008) Back in time: a new systematic proposal for the Bilateria. Philos Trans R Soc Lond B Biol Sci 363:1481–1491Google Scholar
  11. Broun M, Gee L, Reinhardt B, Bode HR (2005) Formation of the head organizer in hydra involves the canonical Wnt pathway. Development 132:2907–2916Google Scholar
  12. Callaerts P, Halder G, Gehring WJ (1997) Pax-6 in development and evolution. Annu Rev Neurosci 20:483–532Google Scholar
  13. Caestro C, Bassham S, Postlethwait J (2005) Development of the central nervous system in the larvacean Oikopleura dioica and the evolution of the chordate brain. Dev Biol 285(2):298–315Google Scholar
  14. Carroll SB, Grenier JK, Weatherbee SD (2001) From DNA to diversity. Blackwell Science, MaldenGoogle Scholar
  15. Chapman JA, Kirkness EF, Simakov O, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D, Disbennett K, Pfannkock C, Sumin N, Sutton GG, Devi Viswanathan L, Walenz B, Goodstein DM, Hellsten U, Kawashima T, Prochnik SE, Putnam NH, Shu S, Blumberg B, Dana CE, Gee L, Kibler DF, Law L, Lindgens D, Martinez DE, Peng J, Wigge PA, Bertulat B, Guder C, Nakamura Y, Ozbek S, Watanabe H, Khalturin K, Hemmrich G, Franke A, Augustin R, Fraune S, Hayakawa E, Hayakawa S, Hirose M, Hwang J-S, Ikeo K, Nishimiya-Fujisawa C, Ogura A, Takahashi T, Steinmetz PRH, Zhang X, Aufschnaiter R, Eder M-F, Gorny A-K, Salvenmoser W, Heimberg AM, Wheeler BM, Peterson KJ, Böttger A, Tishler P, Wolf A, Gojobori T, Remington KA, Strausberg RL, Venter JC, Technau U, Hobmayer B, Bosch TCG, Holstein TW, Fujisawa T, Bode HR, David CN, Rokhsar DS, Steele RE (2010) The dynamic genome of Hydra. Nature 464:592–597Google Scholar
  16. Chiori R, Jager M, Denker E, Wincker P, Da Silva C, Le Guyader H, Manuel M, Quéinnec E (2009) Are Hox genes ancestrally involved in axial patterning? Evidence from the Hydrozoan Clytia hemisphaerica (Cnidaria). PLoS One 4(1):e4231Google Scholar
  17. Davidson EH, Erwin DH (2010) An integrated view of Precambrian eumetazoan evolution. Cold Spring Harb Symp Quant Biol 79:65–80Google Scholar
  18. De RobertisEM(2008) Evo-Devo: variations on ancestral patterning in bilateria. Nature 380:37–40Google Scholar
  19. De Robertis EM, Kuroda H (2004) Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu Rev Cell Dev Biol 20:285–308Google Scholar
  20. De Robertis EM, Sasai Y (1996) A common plan for dorsoventral patterning in bilateria. Nature 380:37–40Google Scholar
  21. Dray N, Tessmar-Raible K, Le Gouar M, Vibert L, Christodoulou F, Schipany K, Guillou A, Zantke J, Snyman H, Béhague J (2010) Hedgehog signaling regulates segment formation in the annelid Platynereis. Science 329(5989):339–342Google Scholar
  22. Edgecombe GD, Giribet G, Dunn CW, Hejnol A, Kristensen RM, Neves RC, Rouse GW, Worsaae K, Sørensen MV (2011) Higher-level metazoan relationships: recent progress and remaining questions. Org Divers Evol 11:151–172Google Scholar
  23. Erwin DH (2008) Macroevolution of ecosystem engineering, niche construction, and diversity. Trends Ecol Evol 23:304–310Google Scholar
  24. Erwin, DH (2009) Early origin of the bilaterian developmental toolkit. Philos Trans R Soc Lond B Biol Sci 364:2253–2261Google Scholar
  25. Erwin DH, Davidson EH (2002) The last common bilaterian ancestor. Development 129(13): 3021–3032Google Scholar
  26. Erwin DH, Valentine JW (2013) The cambrian explosion: the construction of animal biodiversity. Roberts & Co., GreenwoodGoogle Scholar
  27. Erwin DH, Laflamme M, Tweedt SM, Sperling EA, Pisani D, Peterson KJ (2011) The Cambrian Conundrum: early divergence and later ecological success in the early history of animals. Science 334:1091–1097Google Scholar
  28. Fahey B, Degnan BM (2010) Origin of animal epithelia: insights from the sponge genome. Evol Dev 12:601–617Google Scholar
  29. Fahey B, Larroux C, Woodcroft BJ, Degnan BM (2008) Does the high gene density in the sponge NK homeobox gene cluster reflect limited regulatory capacity? Biol Bull 214(3):205–217Google Scholar
  30. Fairclough SR, Chen Z, Kramer E, Zeng Q, Young S, Robertson HM, Begovic E, Richter DJ, Russ C, Westbrook MJ, Manning G, Lang BF, Haas B, Nusbaum C, King N (2013) Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. Genome Biol 14:R15Google Scholar
  31. Finnerty JR, Pang K, Burton P, Paulson D, Martindale MQ (2004) Origins of bilateral symmetry: Hox and Dpp expression in a sea anemone. Science 304:1335–1337Google Scholar
  32. Forêt S, Knack B, Houliston E, Momose T, Manuel M, Quéinnec E, Hayward DC, Ball E, Miller DJ (2010) New tricks with old genes: the genetic basis of novel cnidarian traits. Trends Genet 26(4):154–158Google Scholar
  33. Fortunato S, Adamski M, Bergum B, Guder C, Jordal S, Leininger S, Zwafink C, Rapp HT, Adamska M (2012) Genome-wide analysis of the sox family in the calcareous sponge Sycon ciliatum: multiple genes with unique expression patterns. EvoDevo 3:14Google Scholar
  34. Fritz AE, Ikmi A, Seidel C, Paulson A, Gibson MC (2013) Mechanisms of tentacle morphogenesis in the sea anemone Nematostella vectensis. Development 140:2212–2223Google Scholar
  35. Harcet M, Roller M, Cetkovic H, Peina D, Wiens M, Muller WE, Vlahovicek K (2010) Demosponge EST sequencing reveals a complex genetic toolkit of the simplest metazoans. Mol Biol Evol 27(12):2747–2756Google Scholar
  36. Hejnol A, Martindale MQ (2009) Coordinated spatial and temporal expression of Hox genes during embryogenesis in the acoel Convolutriloba longifissura. BMC Biol 7:65Google Scholar
  37. Holland PWH (2013) Evolution of homeobox genes. WIREs Dev Biol 2:31–45Google Scholar
  38. Hui JHL, Raible F, Korchagina N, Dray N, Samain S, Magdelenat G, Jubin C, Segurens B, Balavoine G, Arendt D, Ferrier DEK (2009) Features of the ancestral bilaterian inferred from Platynereis dumerilii ParaHox genes. BMC Biol 7:43Google Scholar
  39. Ikuta T (2011) Evolution of invertebrate deuterostomes and Hox/ParaHox genes. Genomics Proteomics Bioinformatics 9(3):77–96Google Scholar
  40. Ingham P, Nakano Y, Seger C (2011) Mechanisms and functions of Hedgehog signaling across the metazoa. Nat Rev Genet 12:393–406Google Scholar
  41. Jablonski D, Bottjer DJ (1990) The origin and diversification of major groups: environmental patterns and macroevolutionary lags. In: Taylor PD, Larwood GP (eds) Major evolutionary radiations. Systematics association special, vol 42. Clarendon Press, Oxford, pp 17–57Google Scholar
  42. Jakob W, Sagasser S, Dellaporta S, Holland P, Kuhn K, Schierwater B (2004) The Trox-2 Hox/ParaHox gene of Trichoplax (Placozoa) marks an epithelial boundary. Dev Genes Evol 214(4):170–175Google Scholar
  43. King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, Marr M, Pincus D, Putnam N, Rokas A, Wright KJ, Zuzow R, Dirks W, Good M, Goodstein D, Lemons D, Li W, Lyons JB, Morris A, Nichols S, Richter DJ, Salamov A, Sequencing JGI, Bork P, Lim WA, Manning G, Miller WT, McGinnis W, Shapiro H, Tjian R, Grigoriev IV, Rokhsar D (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451(7180):783–788Google Scholar
  44. Knoll AH (2011) The multiple origins of complex multicellularity. Annu Rev Earth Planet Sci 39:217–239Google Scholar
  45. Knoll AH, Carroll SB (1999) Early animal evolution: emerging views from comparative biology and geology. Science 284:2129–2137Google Scholar
  46. Kraus Y, Fritzenwanker JH, Genikhovich G, Technau U (2007) The blastoporal organiser of a sea anemone. Curr Biol 17:R874–876Google Scholar
  47. Kuo D-H, Weisblat DA (2011) A new molecular logic for BMP-mediated dorsoventral patterning in the leech Helobdella. Curr Biol 21:1281–1288Google Scholar
  48. Larroux C, Luke GN, Koopman P, Rohksar D, Shimeld SM, Degnan BM (2008) Genesis and expansion of metazoan transcription factor gene classes. Mol Biol Evol 25:980–996Google Scholar
  49. Lee PN, Kumburegama S, Marlow HQ, Martindale MQ, Wikramanayake AH (2007) Asymmetric developmental potential along the animal-vegetal axis in the anthozoan cnidarian, Nematostella vectensis, is mediated by Dishevelled. Dev Biol 310:169–186Google Scholar
  50. Leys SP, Riesgo A (2012) Epithelia, an evolutionary novelty of metazoans. J Exp Zool B Mol Dev Evol 318(6):438–447Google Scholar
  51. Leys SP, Cronin TW, Degnan BM, Marshall JN (2002) Spectral sensitivity in a sponge larva. J Comp Physiol A 188:199–202Google Scholar
  52. Love GD, Grosjean E, Stalvie C, Fike DA, Grotzinger JP, Bradley AS, Kelly AE, Bhatia M, Meredith W, Snape CE, Bowring SA, Condon DJ, Summons RE (2009) Fossil steroids record the appearance of Demospongia during the Cryogenian period. Nature 457:718–721Google Scholar
  53. Lowe CJ, Terasaki M, Wu M, Freeman RM Jr, Runft L, Kwan K, Haijo S, Aronowicz J, Lander E, Gruber C, Smith M, Kirschner M, Gerhart J (2006) Dorsoventral patterning in hemichordates: insights into early chordate evolution. PLoS Biol 4(9):e291Google Scholar
  54. Ma X, Hou X, Edgecombe GD, Strausfeld NJ (2012) Complex brain and optic lobes in an early Cambrian arthropod. Nature 490:258–263Google Scholar
  55. Magie CR, Pang K, Martindale MQ (2005) Genomic inventory and expression of Sox and Fox genes in the cnidarian Nematostella vectensis. Dev Genes Evol 215:618–630Google Scholar
  56. Maloof AC, Rose CV, Calmet CC, Beach R, Samuels BM, Erwin DH, Poirier GR, Yao N, Simons FJ (2010) Probable animal body-fossils from pre-Marinoan limestones, South Australia. Nat Geosci 3:653–659Google Scholar
  57. Martinelli C, Spring J (2008) Distinct expression patterns of the two T-box homologues Brachyury and Tbx2/3 in the placozoan Trichoplax adhaerens. Dev Genes Evol 213(10):492–499Google Scholar
  58. Maxwell EK, Ryan JF, Schnitzler CE, Browne WE, Baxevanis AD (2012) MicroRNAs and essential components of the microRNA processing machinery are not encoded in the genome of the ctenophore Mnemiopsis leidyi. BMC Genomics 13:714Google Scholar
  59. Mayr E (1960) The emergence of novelty. In: Tax S (ed) The evolution of life. University of Chicago Press, Chicago, pp 349–380Google Scholar
  60. Miller DJ, Ball EE (2009) The gene complement of the ancestral bilaterian—was Urbilateria a monster? J Biol 8:89Google Scholar
  61. Momose T, Houliston E (2007) Two oppositely localized frizzled RNAs as axis determinants in a cnidarian embryo. PLoS Biol 5:e70Google Scholar
  62. Momose T, Derelle R, Houliston E (2008) A maternally localized Wnt ligand required for axial patterning in the cnidarian Clytia hemisphaerica. Development 135:2105–2113Google Scholar
  63. Momose T, Kraus Y, Houliston E (2012) A conserved function for Strabismus in establishing planar cell polarity in the ciliated ectoderm during cnidarian larval development. Development 139:4375–4382Google Scholar
  64. Nichols SA, Dirks W, Pearse JS, King N (2006) Early evolution of animal cell signaling and adhesion genes. Proc Natl Acad Sci U S A 103(33):12451–12456Google Scholar
  65. Nichols SA, Roberts BW, Richter DJ, Fairclough SR, King N (2012) Origin of metazoan cadherin diversity and the antiquity of the classical cadherin/beta-catenin complex. Proc Natl Acad Sci U S A 109(32):13046–13051Google Scholar
  66. Nosenko T, Schreiber F, Adamska M, Adamski M, Eitel M, Hammel J, Maldonado M, Muller WEG, Nickel M, Schierwater B, Vacelet J, Wiens M, Wörheide G. (2013) Deep metazoan phylogeny: when different genes tell different stories. Mol Phylogenet Evol 67:223–233Google Scholar
  67. Ogura A, Ikeo K, Gojobori T (2005) Estimation of ancestral gene set of bilaterian animals and its implication to dynamic change of gene content in bilaterian evolution. Gene 345(1):65–71Google Scholar
  68. Pang K, Ryan JF, Baxevanis AD, Martindale MQ (2011) Evolution of the TGF-beta signaling pathway and its potential role in the ctenophore, Mnemiopsis leidyi. PLoS One 6(9):e24152Google Scholar
  69. Pani AM, Mullarkey EE, Aronowicz J, Assimacopoulos S, Grove EA, Lowe CJ (2012) Ancient deuterostome origins of vertebrate brain signaling centres. Nature 483:289–296Google Scholar
  70. Parfrey LM, Lahr DJG (2013) Multicellularity arose several times in the evolution of eukaryotes. Bioessays 35:339–347Google Scholar
  71. Petersen CP, Reddien PW (2009) Wnt signaling and the polarity of the primary body axis. Cell 139:1056–1068Google Scholar
  72. Philippe H, Brinkmann H, Copley RR, Moroz LL, Nakano H, Poustka AJ, Wallberg A, Peterson KJ, Telford MJ (2011a) Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470:255–258Google Scholar
  73. Philippe H, Brinkmann H, Lavrov DV, Littlewood DTJ, Manuel M, Wörheide G, Baurain D (2011b) Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol 9(3):e1000602Google Scholar
  74. Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV, Jurka J, Genikhovich G, Grigoriev IV, Lucas SM, Steele RE, Finnerty JR, Technau U, Martindale MQ, Rokhsar DS (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86–96Google Scholar
  75. Ramos OM, Barker D, Ferrier DEK (2012) Ghost loci imply Hox and ParaHox existence in the last common ancestor of animals. Curr Biol 22:1951–1956Google Scholar
  76. Richards GS, Degnan BM (2012) The expression of Delta ligands in the sponge Amphimedon queenslandica suggest an ancient role for Notch signaling in metazoan development. EvoDevo 3:1–15Google Scholar
  77. Ringrose JH, van den Toorn HWP, Eitel M, Post H, Neerincx P, Schierwater B, Altelaar AFM, Heck AJR (2013) Deep proteome profiling of Trichoplax adhaerens reveals remarkable features at the origin of metazoan multicellularity. Nat Commun 4(1408):1–7Google Scholar
  78. Rivera AS, Ozturk N, Fahey B, Plachetzki DC, Degnan BM, Sancar A, Oakley TH (2012) Blue-light-receptive cryptochrome is expressed in a sponge eye lacking neurons and opsin. J Exp Biol 215:1278–1286Google Scholar
  79. Rivera A, Winters I, Rued A, Ding S, Posfai D, Cieniewicz B, Cameron K, Gentile L, Hill A (2013) The evolution and function of the Pax/Six regulatory network in sponges. Evol Dev 15(3):186–196Google Scholar
  80. Robinson JM, Sperling EA, Bergum B, Adamski M, Nichols SA, Adamska M, Peterson KJ (2013) The identification of microRNAs in Calcisponges: Independent eolution of microRNAs in basal metazoans. J Exp Zool B Mol Dev Evol 320:84–93Google Scholar
  81. Rokas A (2008) The origins of multicellularity and the early history of the genetic toolkit for animal development. Annu Rev Genet 42:235–251Google Scholar
  82. Rota-Stabelli O, Daley AC, Pisani D (2013) Molecular timetrees reveal a Cambrian colonization of land and a new scenario for Ecdysozoan evolution. Curr Biol 23:392–398Google Scholar
  83. Röttinger E, Dahlin P, Martindale MQ (2012) A framework for the establishment of a cnidarian gene regulatory network for “endomesoderm” specification: the inputs of β-catenin/TCF signaling. PLoS Genet 8(12):e1003164Google Scholar
  84. Rowland SJ (2001) Archaeocyaths—a history of phylogenetic interpretation. J Paleontol 75:1065–1078Google Scholar
  85. Ryan JF, Pang K, Mullikin JC, Martindale MQ, Baxevanis AD, Progra NCS (2010) The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa. EvoDevo 1:9.Google Scholar
  86. Ryan JF, Pang K, Schnitzler CE, Nguyen AD, Moreland RT, Simmons DK, Koch BJ, Francis WR, Havlak P, NISC Comparative Sequencing Program, Smith SA, Putnam NH, Haddock SHD, Dunn CW, Wolfsberg TG, Mullikin JC, Martindale MQ, Baxevanis AD (2013) The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342:124592Google Scholar
  87. 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(44):18592–18597Google Scholar
  88. Schierwater B, Kamm K (2010) The early evolution of Hox genes: a battle of believe? In: Deutsch J (ed) Hox Genes’ studies from the 20th to the 21st century, advances in experimental medicine and biology, vol 689. Landes Bioscience, New York, pp 81–90Google Scholar
  89. Schierwater B, Eitel M, Osigus HJ, von der Chevallerie K, Bergmann T, Hadrys H, Cramm M, Heck L, Jakob W, Lang MR, DeSalle R (2011) Trichoplax and Placozoa: one of the crucial keys to understanding metazoan evolution. In: DeSalle R, Schierwater B (eds) Key transitions in animal evolution. Science Publishers, Enfield, pp 289–326Google Scholar
  90. Sebé-Pedrós A, Ruiz-Trillo I, de Mendoza A, Lang BF, Degnan BM (2011) Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol Biol Evol 28(3):1241–1254Google Scholar
  91. Sebé-Pedrós A, Ariza-Cosano A, Weirauch MT, Leininger S, Yang A, Torruella G, Adamski M, Adamska M, Hughes TR, Gómez-Skarmeta JL, Ruiz-Trillo I (2013) Early evolution of the T-box transcription factor family. Proc Natl Acad Sci U S A 110(40):16050–16055Google Scholar
  92. Shenk MA, Steel MA (1994) A molecular snapshot of the metazoan ‘Eve’. Trends Biochem Sci 18:459–463Google Scholar
  93. Simakov O, Marletaz F, Cho S-J, Edsinger-Gonzales E, Havlak P, Hellsten U, Kuo D-H, Larsson T, Lv J, Arendt D, Savage R, Osoegawa K, de Jong P, Grimwood J, Chapman JA, Shapiro H, Aerts A, Otillar RP, Terry AY, Boore JL, Grigoriev IV, Lindberg DR, Seaver EC, Weisblat DA, Putnam NH, Rokhsar DS (2013) Insights into bilaterian evolution from three spiralian genomes. Nature 493:526–532Google Scholar
  94. Sinigaglia C, Busengdal H, Leclère L, Technau U, Rentzsch F (2013) The bilaterian head patterning gene six3/6 controls aboral domain development in a cnidarian. PLoS Biol 11(2):e1001488Google Scholar
  95. Sperling EA, Vinther J (2010) A placozoan affinity for Dickinsonia and the evolution of late Proterozoic metazoan feeding modes. Evol Dev 12:201–209Google Scholar
  96. Sperling EA, Pisani D, Peterson KJ (2007) Poriferan paraphyly and its implications for Precambrian palaeobiology. In: Vickers-Rich P, Komarower P (eds) The rise and fall of the Ediacaran biota, geological society special publication, vol 286. Geological Society of London, London, pp 355–368Google Scholar
  97. Sperling EA, Peterson KJ, Pisani D (2009) Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of eumetazoa. Mol Biol Evol 26:2261–2274Google Scholar
  98. Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, Kuo A, Mitros T, Salamov A, Carpenter ML, Signorovitch AY, Moreno MA, Kamm K, Grimwood J, Schmutz J, Shapiro H, Grigoriev IV, Buss LW, Schierwater B, Dellaporta SL, Rokhsar DS (2008) The Trichoplax genome and the nature of placozoans. Nature 454(7207):955–960Google Scholar
  99. Srivastava M, Larroux C, Lu DR, Mohanty K, Chapman J, Degnan BM, Rokhsar DS (2010a) Early evolution of the LIM homeobox gene family. BMC Biol 8(4):1–13Google Scholar
  100. Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier MEA, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki DC, Zhai YF, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson DJ, Leys SP, Shu SQ, Woodcroft BJ, Vervoort M, Kosik KS, Manning G, Degnan BM, Rokhsar DS (2010b) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466(7307):720–723Google Scholar
  101. Steele RE, David CN, Technau U (2011) A genomic view of 500 million years of cnidarian evolution. Trends Genet 27(1):7–13Google Scholar
  102. Steinmetz PRH, Kraus JEM, Larroux C, Hammel JU, Amon-Hassenzahl A, Houliston E, Wörheide G, Nickel M, Degnan BM, Technau U (2012) Independent evolution of striated muscles in cnidarians and bilaterians. Nature 487(7406):231–234Google Scholar
  103. Stromberg CAE (2005) Decoupled taxonomic radiation and ecological expansion of open-habitat grasses in the Cenozoic of North America. Proc Natl Acad Sci U S A 102:11980–11984Google Scholar
  104. Sullivan JC, Kalaitzidis D, Gilmore TD, Finnerty JR (2006) Rel homology domain-containing transcription factors in the cnidarian Nematostella vectensis. Dev Genes Evol 217:63–72Google Scholar
  105. Valentine JW, Jablonski D, Erwin DH (1999) Fossils, molecules and embryos: new perspectives on the Cambrian explosion. Development 126:851–859Google Scholar
  106. Vij S, Rink JC, Ho HK, Babu D, Eitel M, Narasimhan V, Tiku V, Westbrook J, Schierwater B, Roy S (2012) Evolutionarily ancient association of the FoxJ1 transcription factor with the motile ciliogenic program. PLoS Genet 8(11):e1003019Google Scholar
  107. Winchell CJ, Jacobs DK (2013) Expression of the Lhx genes apterous and lim1 in an errant polychaete: implications for bilaterian appendage evolution, neural development, and muscle diversification. EvoDevo 4:4Google Scholar
  108. Winchell CJ, Valencia JE, Jacobs DK (2010) Expression of Distal-less, dachshund, and optomotor blind in Neanthes arenaceodentata Annedlida, Nereididae) does not support homology of appendage-forming mechanisms across the Bilateria. Dev Genes Evol 220:275–295Google Scholar
  109. Windsor PJ, Leys SP (2010) Wnt signaling and induction in the sponge aquiferous system: evidence for an ancient origin of the organizer. Evol Dev 12(5):484–493Google Scholar
  110. Wyder S, Kriventseva EV, Schröder R, Kadowaki T, Zdobnov EM (2007) Quantification of ortholog losses in insects and vertebrates. Genome Biol 8(11):R242Google Scholar
  111. Xavier-Neto J, Castro RA, Sampaio AC, Azambuja AP, Castillo HA, Cravo RM, Simões-Costa MS (2007) Parallel avenues in the evolution of hearts and pumping organs. Cell Mol Life Sci 64:719–734Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Department of PaleobiologyNational Museum of Natural HistoryWashingtonUSA
  2. 2.Behavior, Ecology, Evolution, & SystematicsUniversity of MarylandMDUSA

Personalised recommendations