Development Genes and Evolution

, Volume 217, Issue 8, pp 585–592 | Cite as

Ontogeny of the holothurian larval nervous system: evolution of larval forms

  • Cory D. Bishop
  • Robert D. BurkeEmail author
Original Article


Echinoderm larvae share numerous features of neuroanatomy. However, there are substantial differences in specific aspects of neural structure and ontogeny between the dipleurula-like larvae of asteroids and the pluteus larvae of echinoids. To help identify apomorphic features, we have examined the ontogeny of the dipleurula-like auricularia larva of the sea cucumber, Holothuria atra. Neural precursors arise in the apical ectoderm of gastrulae and appear to originate in bilateral clusters of cells. The cells differentiate without extensive migration, and they align with the developing ciliary bands and begin neurogenesis. Neurites project along the ciliary bands and do not appear to extend beneath either the oral or aboral epidermis. Apical serotonergic cells are associated with the preoral loops of the ciliary bands and do not form a substantial commissure. Paired, tripartite connectives form on either side of the larval mouth that connect the pre-oral, post-oral, and lateral ciliary bands. Holothurian larvae share with hemichordates and bipinnariae a similar organization of the apical organ, suggesting that the more highly structured apical organ of the pluteus is a derived feature. However, the auricularia larva shares with the pluteus larva of echinoids several features of neural ontogeny. Both have a bilateral origin of neural precursors in ectoderm adjacent to presumptive ciliary bands, and the presumptive neurons move only a few cell diameters before undergoing neurogenesis. The development of the holothurian nervous systems suggests that the extensive migration of neural precursors in asteroids is a derived feature.


Ontogeny Neural development Echinoderm Evolution 



This study was supported in part by a discovery grant from NSERC (Canada) to RDB and an NSERC post-doctoral fellowship to CDB. Mark Martindale (University of Hawaii) and Michael Hadfield (University of Hawaii) are gratefully acknowledged for supporting aspects of this work. Thurston Lacalli provided helpful comments on the manuscript.

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  1. Beer AJ, Moss C, Thorndyke M (2001) Development of serotonin-like and SALMFamide-like immunoreactivity in the nervous system of the sea urchin Psammechinus miliaris. Biol Bull 200:268–280PubMedCrossRefGoogle Scholar
  2. Bisgrove BW, Burke RD (1986) Development of serotonergic neurons in embryos of the sea urchin Strongylocentrotus purpuratus. Dev Growth Differ 28:569–574CrossRefGoogle Scholar
  3. Bisgrove BW, Burke RD (1987) Development of the nervous system of the pluteus larva of Strongylocentrotus droebachiensis. Cell Tissue Res 248:335–343CrossRefGoogle Scholar
  4. Bishop CD, Brandhorst BP (2007) Development of nitric oxide synthase-defined neurons in the sea urchin larval ciliary band and evidence for a chemosensory function during metamorphosis. Dev Dyn 236:1535–1546PubMedCrossRefGoogle Scholar
  5. Burke RD (1978) The structure of the nervous system of the pluteus larva of Strongylocentrotus purpuratus. Cell Tissue Res 191:233–247PubMedCrossRefGoogle Scholar
  6. Burke RD (1983) Structure of the larval nervous system of Pisaster ochraceus, (Echinodermata:Asteroidea). J Morphol 178:23–35CrossRefGoogle Scholar
  7. Burke RD, Brand DW, Bisgrove BW (1986) Structure of the nervous system of the auricularia larva of Parastichopus californicus. Biol Bull 170:450–460CrossRefGoogle Scholar
  8. Burke RD, Osborne L, Wang D, Murabe N, Yaguchi S, Nakajima Y (2006a) Neuron-specific expression of a synaptotagmin gene in the sea urchin Strongylocentrotus purpuratus. J Comp Neurol 496:244–251PubMedCrossRefGoogle Scholar
  9. Burke RD, Angerer LM, Elphick MR, Humphrey GW, Yaguchi S, Kiyama T, Liang S, Mu X, Agca C, Klein WH, Brandhorst BP, Rowe M, Wilson K, Churcher AM, Taylor JS, Chen N, Murray G, Wang D, Mellott D, Olinski R, Hallbook F, Thorndyke MC (2006b) A genomic view of the sea urchin nervous system. Dev Biol 300:434–460PubMedCrossRefGoogle Scholar
  10. Byrne M, Sewell MA, Selvakumaraswamy P, Prowse TAA (2006) The larval apical organ in the holothuroid chiridoata gigas (Apodida): inferences on evolution of the ambulacraraian larval nervous system. Biol Bull 211:95–100PubMedGoogle Scholar
  11. Chee F, Byrne M (1999) Development of the larval serotonergic nervous system in the sea star Patiriella regularis as revealed by confocal imaging. Biol Bull 197:123–131CrossRefGoogle Scholar
  12. Chen CP, Tseng CH, Chen BY (1995) The development of the catecholaminergic nervous system in starfish and sea cucumber larvae. Zool Stud 34:248–256Google Scholar
  13. Chia FS, Burke RD, Koss R, Mladenov PV, Rumrill SS (1986) Fine structure of the doliolaria larva of the feather star Florometra serratissma with special emphasis on the nervous system. J Morphol 189:99–120CrossRefGoogle Scholar
  14. Cisternas PA, Byrne M (2003) Peptidergic and serotonergic immunoreactivity in the metamorphosing ophiopluteus of Ophiactis resiliens (Echinodermata, Ophiuroidea). Invertebr Biol 122:177–185CrossRefGoogle Scholar
  15. David B, Mooi R (1997) Major events in the evolution of echino-derms viewed by the light of embryology. In: Mooi R, Telford M (eds) Echindoerms: San Francisco. Balkema, Rotterdam, pp 21–28Google Scholar
  16. Hay-Schmidt A (2000) The evolution of the serotonergic nervous system. Proc R Soc Lond B Biol Sci 267:1071–1079CrossRefGoogle Scholar
  17. Lacalli TC (1994) Apical organs, epithelial domains, and the origin of the chordate central nervous system. Am Zool 34:533–541Google Scholar
  18. Lacalli TC, Kelly SJ (2002) Anterior neural centres in echinoderm bipinnaria and auricularia larvae: cell types and organization. Acta Zool 83:99–110CrossRefGoogle Scholar
  19. Littlewood DTJ, Smith AB, Clough KA, Emson RH (1997) The interrelationships of the echinoderm classes: Morphological and molecular evidence. Biol J Linn Soc 61:409–438CrossRefGoogle Scholar
  20. Moss C, Burke RD, Thorndyke MC (1994) Immunocytochemical localization of the neuropeptide-S1 and serotonin in larvae of the starfish Pisaster ochraceus and Asterias rubens. J Mar Biol Assoc UK 74:61–71CrossRefGoogle Scholar
  21. Nakajima Y (1986a) Presence of a ciliary patch in preoral epithelium of sea urchin plutei. Dev Growth Differ 28:243–249CrossRefGoogle Scholar
  22. Nakajima Y (1986b) Development of the nervous system of sea urchin embryos—formation of the ciliary band and the appearance of 2 types of ectoneural cells in the pluteus. Dev Growth Differ 28:531–542CrossRefGoogle Scholar
  23. Nakajima Y (1988) Serotonergic nerve cells of starfish larvae. In: Burke R, Mladenov PV, Lambert P, Parsley RL (eds) Echinoderm biology. Balkema, Rotterdam, pp 235–239Google Scholar
  24. Nakajima Y, Kaneko H, Murray G, Burke RD (2004) Divergent patterns of neural development in larval echinoids and asteroids. Evolut Develop 6:95–104CrossRefGoogle Scholar
  25. Nakano H, Murabe N, Amemiya S, Nakajima Y (2006) Nervous system development of the sea cucumber Stichopus japonicus. Dev Biol 292:205–212PubMedCrossRefGoogle Scholar
  26. Nezlin LP, Yushin VV (2004) Structure of the nervous system in the tornaria larva of Balanoglossus proterogonius (Hemichordata: Enteropneusta) and its phylogenetic implications. Zoomorphology 123:1–13CrossRefGoogle Scholar
  27. Nielsen C (1998) Origin and evolution of animal life cycles. Biol Rev 73:125–155CrossRefGoogle Scholar
  28. Nielsen C (2005) Larval and adult brains. Evolut Develop 7:483–489CrossRefGoogle Scholar
  29. Smith MJ, Arndt A, Gorski S, Fajber E (1993) The phylogeny of echinoderm classes based on mitochondrial gene arrangements. J Mol Evol 36:545–554PubMedCrossRefGoogle Scholar
  30. Strathmann R (1978) The evolution and loss of feeding larval stages of marine invertebrate larvae. 32:894–906Google Scholar
  31. Strathmann RR (1993) Hypotheses on the origins of marine larvae. Ann Rev Ecolog Syst 24:89–117CrossRefGoogle Scholar
  32. Strathmann RR, Eernisse DJ (1994) What molecular phylogenies tell us about the evolution of larval forms. Am Zool 34:502–512Google Scholar
  33. Yaguchi S, Yaguchi J, Burke RD (2006) Specification of ectoderm restricts the size of the animal plate and patterns neurogenesis in sea urchin embryos. Development 133:2337–2346PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Kewalo Marine LaboratoryUniversity of HawaiiHonoluluUSA
  2. 2.Department of Biology and Biochemistry/MicrobiologyUniversity of VictoriaVictoriaCanada

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