Model Systems for Exploring the Evolutionary Origins of the Nervous System

  • Karri M. Haen WhitmerEmail author
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 65)


The development of nervous systems can be seen as one of the key transitions in animal evolution, allowing the efficient integration of sensory input and motor output and the expedient transmission of impulses over relatively long distances inside an organism. With the increased availability of genome sequences for animals at the base of the metazoan phylogenetic tree, two alternative hypotheses have been proposed regarding nervous system evolutionary origins, ultimately prompting a debate whether an enormously complicated system like the nervous system could have evolved more than once. This review summarizes what is currently known about nervous system origins, concentrating on the evolution of synapse components, with respect to phylogenetic knowledge of early diverging animal groups, comprising members of the Porifera, Ctenophora, Placozoa, and Cnidaria.


  1. Adams EDM, Goss GG, Leys SP (2010) Freshwater sponges have functional, sealing epithelia with high transepithelial resistance and negative transepithelial potential. PLoS One 5(11):e15040CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alié 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. Scholar
  3. Bosch TCG, Klimovich A, Domazet-Lošo T et al (2017) Back to the basics: Cnidarians start to fire. Trends Neurosci 40(2):92–105. Scholar
  4. Burkhardt P (2015) The origin and evolution of synaptic proteins–Choanoflagellates lead the way. J Exp Biol 218:506–514. Scholar
  5. Chapman J et al (2010) The dynamic genome of Hydra. Nature 464:592–596. Scholar
  6. Collins AG (1998) Evaluating multiple alternative hypotheses for the origin of Bilateria: an analysis of 18S rRNA molecular evidence. Proc Natl Acad Sci USA 95:15458–15463CrossRefPubMedGoogle Scholar
  7. da Silva FB, Muschner VC, Bonatto SL (2007) Phylogenetic position of Placozoa based on large subunit (LSU) and small subunit (SSU) rRNA genes. Genet Mol Biol 30(1):127–132CrossRefGoogle Scholar
  8. Dellaporta SL, Xu A, Sagasser S, Jakob W, Moreno MA, Buss LW, Schierwater B (2006) Mitochondrial genome of Trichoplax adhaerens supports Placozoa as the basal lower Metazoan phylum. Proc Natl Acad Sci USA 103:8751–8756CrossRefPubMedGoogle Scholar
  9. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD et al (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749. Scholar
  10. Dunn CW, Leys SP, Haddock SHD (2015) The hidden biology of sponges and ctenophores. Trends Ecol Evol 30(5):282–291CrossRefPubMedGoogle Scholar
  11. Eitel M, Osigus H-J, DeSalle R, Schierwater B (2013) Global diversity of the Placozoa. PLoS One 8(4):e57131CrossRefPubMedPubMedCentralGoogle Scholar
  12. Elliott G, Leys SP (2010) Evidence for glutamate, GABA and NO in coordinating behaviour in the sponge, Ephydatia muelleri (Demospongiae, Spongillidae). J Exp Biol 213:2310–2321CrossRefPubMedGoogle Scholar
  13. Ellwanger K, Eich A, Nickel M (2007) GABA and glutamate specifically induce contractions in the sponge Tethya wilhelma. J Comp Physiol A 193(1):1–11. Scholar
  14. 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(6059):1091–1097CrossRefPubMedGoogle Scholar
  15. Garm A, Mori S (2009) Multiple photoreceptor systems control the swim pacemaker activity in box jellyfish. J Exp Biol 212:3951–3960CrossRefPubMedGoogle Scholar
  16. Hejnol A et al (2009) Assessing the root of Bilaterian animals with scalable phylogenomic methods. Proc R Soc B 276:4261–4270CrossRefPubMedGoogle Scholar
  17. Hooper JNA, van Soest RWM (2002) Systema Porifera: a guide to the classification of sponges. Kluwer Academic, DordrechtCrossRefGoogle Scholar
  18. Jékely G, Paps J, Nielsen C (2015) The phylogenetic position of ctenophores and the origin(s) of nervous systems. Evodevo 6:1CrossRefPubMedPubMedCentralGoogle Scholar
  19. Kass-Simon G, Pierobon P (2007) Cnidarian chemical neurotransmission, an updated overview. Comp Biochem Physiol A Mol Integr Physiol 146:9–25CrossRefPubMedGoogle Scholar
  20. Koizumi O, Sato N, Goto C (2004) Chemical anatomy of hydra nervous system using antibodies against hydra neuropeptides: a review. Hydrobiologia 530/531:41–47CrossRefGoogle Scholar
  21. Krishnan A, Dnyansagar R, Almén MS, Williams MJ, Fredriksson R, Manoj N, Schiöth HB (2014) The GPCR repertoire in the demosponge Amphimedon queenslandica: insights into the GPCR system at the early divergence of animals. BMC Evol Biol 14:270CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kristan WB (2016) Early evolution of neurons. Curr Biol 26:R949–R954. Scholar
  23. Leys SP (2015) Elements of a ‘nervous system’ in sponges. J Exp Biol 218(4):581–591CrossRefPubMedGoogle Scholar
  24. Leys SP, Degnan BM (2001) Cytological basis of photoresponsive behavior in a sponge larva. Biol Bull 201(3):323–338CrossRefPubMedGoogle Scholar
  25. Leys SP, Nichols SA, Adams EDM (2009) Epithelia and integration in sponges. Integr Comp Biol 49(2):167–177CrossRefPubMedGoogle Scholar
  26. Love GD, Grosjean E, Stalvies C, Fike DA, Grotzinger JP, Bradley AS et al (2009) Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457:718–721CrossRefPubMedGoogle Scholar
  27. Marlow H, Arendt D (2014) Evolution: ctenophore genomes and the origin of neurons. Curr Biol 24:R757–R761. Scholar
  28. Mills CE (1998) Phylum Ctenophora: list of all valid species names. Electronic internet document available at Published by the author, last updated June, 2017
  29. Moroz L, Kohn AB (2015) Unbiased view of synaptic and neuronal gene complement in ctenophores: are there pan-neuronal and pan-synaptic genes across Metazoa? Integr Comp Biol 55(6):1028–1049PubMedPubMedCentralGoogle Scholar
  30. Moroz LL et al (2014) The ctenophore genome and the evolutionary origins of neural systems. Nature 510:109–114. Scholar
  31. Philippe H, Derelle R, Lopez P, Pick K, Borchiellini C, Boury-Esnault N, Vacelet J, Renard E, Houiliston E, Quéinnec E et al (2009) Phylogenomics revives traditional views on deep animal relationships. Curr Biol 19:1–7. Scholar
  32. Pick KS, Philippe H, Schreiber F, Erpenbeck D, Jackson DJ, Wrede P, Wiens M, Alié A, Morgenstern B, Manuel M, Wörheide G (2010) Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol Biol Evol 27:1983–1987. Scholar
  33. Pisani D, Pett W, Dohrmann M, Feuda R, Rota-Stabelli O, Philippe H, Lartillot N, Wörheide G (2015) Genomic data do not support comb jellies as the sister group to all other animals. Proc Natl Acad Sci 112(50):15402–15407CrossRefPubMedGoogle Scholar
  34. Putnam NH et al (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317(5834):86–94. Scholar
  35. Ryan JF et al (2013) The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342(6164):1242592. Scholar
  36. Sakarya O, Armstrong KA, Adamska M, Adamski M, Wang IF, Tidor B, Degnan BM, Oakley TH, Kosik KS (2007) A post-synaptic scaffold at the origin of the animal kingdom. PLoS One 2:e506CrossRefPubMedPubMedCentralGoogle Scholar
  37. Schierwater B, Eitel M, Jakob W, Osigus H-J, Hadrys H, Dellaporta SL et al (2009) Concatenated analysis sheds light on early Metazoan evolution and fuels a modern “urmetazoon” hypothesis. PLoS Biol 7:e1000020. Scholar
  38. Schubert, P. (1993) Trichoplax adhaerens (Phylum Placozoa) has cells that react with antibodies against the neuropeptide RFAmide. in: Acta zoologica. Blackwell Science, Oxford 74:2, p. 115.Google Scholar
  39. Senatore A, Raiss H, Le P (2016) Physiology and evolution of voltage-gated calcium channels in early diverging animal phyla: Cnidaria, Placozoa, Porifera and Ctenophora. Front Physiol 7:481CrossRefPubMedPubMedCentralGoogle Scholar
  40. Senatore A, Reese TS, Smith CL (2017) Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses. J Exp Biol 220:3381–3390. Scholar
  41. Shaham S (2010) Chemosensory organs as models of neuronal synapses. Nat Rev Neurosci 11(3):212–217. Scholar
  42. Simion P, Philippe H, Baurain D, Jager M, Richter DJ, Di Franco A, Roure B, Satoh N, Queinnec E, Ereskovsky A et al (2017) A large and consistent phylogenomic dataset supports sponges as the sister group to all other animals. Curr Biol 27(7):958–967CrossRefPubMedGoogle Scholar
  43. Simpson TL (1984) The cell biology of sponges. Springer, New YorkCrossRefGoogle Scholar
  44. Skogh C, Garm A, Nilsson DE, Ekström P (2006) Bilaterally symmetrical rhopalial nervous system of the box jellyfish Tripedalia cystophora. J Morphol 267:1391–1405CrossRefPubMedGoogle Scholar
  45. Smith CL, Varoqueaux F, Kittelmann M et al (2014) Novel cell types, neurosecretory cells and body plan of the early-diverging Metazoan, Trichoplax adhaerens. Curr Biol 24(14):1565–1572. Scholar
  46. Srivastava M et al (2008) The Trichoplax genome and the nature of Placozoans. Nature 454:955–960. Scholar
  47. 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 Y, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson DJ, Leys SP, Shu S, Woodcroft BJ, Vervoort M, Kosik KS, Manning G, Degnan BM, Rokhsar DS (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466(7307):720–726CrossRefPubMedPubMedCentralGoogle Scholar
  48. Stanley GD, Stürmer W (1983) The first fossil ctenophore from the lower Devonian of West Germany. Nature 303:518–520CrossRefGoogle Scholar
  49. Stanley GD, Stürmer W (1989) A new fossil ctenophore discovered by X-rays. Nature 327:61–63Google Scholar
  50. Südhof TC (2012) The presynaptic active zone. Neuron 75(1):11–25CrossRefPubMedPubMedCentralGoogle Scholar
  51. Watanabe H, Fujisawa T, Holstein TW (2009) Cnidarians and the evolutionary origin of the nervous system. Dev Growth Differ 51:167–183CrossRefPubMedGoogle Scholar
  52. Yin Z et al (2015) Sponge grade body fossil with cellular resolution dating 60 Myr before the Cambrian. Proc Natl Acad Sci USA 112:E1453–E1460PubMedGoogle Scholar
  53. Ziff EB (1997) Enlightening the postsynaptic density. Neuron 19(6):1163–1174CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Genetics, Development & Cell BiologyIowa State UniversityAmesUSA

Personalised recommendations