Abstract
The development of nervous system (NS) in the non-feeding vestibula larva of the sea urchin, Holopneustes purpurescens, and the feeding echinopluteus larva of Hemicentrotus pulcherrimus was examined by focusing on fate during metamorphosis. In H. purpurescens, the serotonergic NS (SerNS) appeared simultaneously and independently in larval tissue and adult rudiment, respectively, from 3-day post-fertilization. In 4-day vestibulae, an expansive aboral ganglion (450 × 100 μm) was present in the larval mid region that extended axons toward the oral ectoderm. These axons diverged near the base of the primary podia. An axonal bundle connected with the primary podia and the rim of vestopore on the oral side. Thus, the SerNS of the larva innervated the rudiment at early stage of development of the primary podia. This innervation was short-lived, and immediately before metamorphosis, it disappeared from the larval and adult tissue domains, whereas non-SerNS marked by synaptotagmin remained. The NS of 1-month post-fertilization plutei of H. pulcherrimus comprised an apical ganglion (50 × 17 μm) and axons that extended to the ciliary bands and the adult rudiment (AR). A major basal nerve of serotonergic and non-serotonergic axons and a minor non-serotonergic nerve comprised the ciliary band nerve. In 3-month plutei, axonal connection among the primary podia in the neural folds completed. The SerNS never developed in the AR. Thus, there was distinctive difference between feeding- and non-feeding larvae of the above sea urchins with respect to SerNS and the AR.
Similar content being viewed by others
References
Bisgrove BW, Burke RD (1986) Development of the nervous system of the pluteus larva of Strongylocentrotus purpuratus. Dev Growth Differ 28:569–574
Bisgrove BW, Raff RA (1989) Evolutionary conservation of the larval serotonergic nervous system in a direct developing sea urchin. Dev Growth Differ 31:363–370
Brown M, Keynes R, Lumsden A (2001) The developing brain. Oxford University Press, New York
Burke RD, Osborne L, Wang D, Murabe N, Yaguchi S, Nakajima Y (2006) Neuron-specific expression of a synaptotagmin gene in the sea urchin Strongylocentrotus purpuratus. J Comp Neurol 496:244–251
Byrne M, Cisternas P (2002) Development and distribution of the peptidergic system in larval and adult Paririella: comparison of the sea star bilateral and radial nervous systems. J Comp Neurol 451:101–114
Byrne M, Emlet RB, Cerra A (2001) Ciliated band structure in planktotrophic and lecithotrophic larvae of Heliocidaris species (Echinodermata: Echinoidea): a demonstration of conservation and change. Acta Zool (Stockh) 82:189–199
Byrne M, Nakajima Y, Chee FC, Burke RD (2007) Apical organs in echinoderm larvae—insights into larval evolution in the Ambulacraria. Evolut Develop 9:432–445
De Felipe J (1993) Neocortical neuronal diversity: chemical heterogeneity revealed by colocalization studies of classic neurotransmitters, neuropeptides, calcium-binding proteins, and cell surface molecules. Cereb Cortex 3:273-289
Ferkowicz MJ, Raff RA (2001) Wnt gene expression in sea urchin development: Heterochronies associated with the evolution of developmental mode. Evolut Develop 3:24–33
Hay-Schmidt A (2000) The evolution of the serotonergic nervous system. Proc R Soc Lond B Biol Sci 267:1071–1079
Jeffery C, Emlet RB, Littlewood DTJ (2003) Macroevolutionary consequences of developmental mode in temnopleurid echinoids from the tertiary of southern Australia. Evolution 57:1031–1048
Jéquiter E, Lovenberg W, Sjoerdsma A (1967) Tryptophan hydroxylase inhibition: the mechanism by which p-chlorophenylalanine depletes rat brain serotonin. Mol Pharmacol 3:274–278
Kano YT, Komatsu M (1978) Development of the sea-star, Asterina batheri Goto. Dev Growth Differ 20:107–114
Katow H (2008) Spatio-temporal expression of a Netrinb homolog in the sea urchin Hemicentrotus pulcherrimus (HpNetrin) during serotonergic axon extension. Int J Dev Biol 52:1077–1088
Katow H, Yaguchi S, Kiyomoto M, Washio M (2004) The 5-HT receptor cell is a new member of secondary mesenchyme cell descendants and forms a major blastocoelar network in sea urchin larvae. Mech Dev 121:325–337
Katow H, Yaguchi S, Kyozuka K (2007) Serotonin stimulates [Ca2+]i elevation in ciliary ectodermal cells of echinoplutei through a serotonin receptor cell network in the blastocoel. J Exp Biol 210:403–412
Morris VB (1995) Apluteal development of the sea urchin Holopneustes purpurescens Agassis (Echinodermata: Echinoidea: Euechinoidea). Zool J Linn Soc 114:349–364
Nakajima Y, Kaneko H, Murray G, Burke RD (2004) Divergent patterns of neural development in larval echinoids. Evol Dev 6:95–104
Raff RA, Byrne M (2006) The active evolutionary lives of echinoderm larvae. Heredity 97:244–252
Riaz SS, Theofilopoulos S, Jauniaux E, Stern GM, Bradford HF (2004) The differentiation potential of human foetal neuronal progenitor cells in vitro. Dev Brain Res 153:39–51
Strathmann RR (1988) Larvae, phylogeny, and von Baer’s Law. In: Paul CRC, Smith AB (eds) Echinoderm phylogeny and evolutionary biology. Clarendon, Oxford, pp 53–68
Vilinski JT, Vilinski JC, Byrne M, Raff RA (2002) Convergent maternal provisioning and life-history evolution in echinoderms. Evolution 56:1764–1775
Yaguchi S, Katow H (2003) Expression of tryptophan 5-hydroxylase gene during sea urchin neurogenesis and role of serotonergic nervous system in larval behavior. J Comp Neurol 466:219–229
Yaguchi S, Kanoh K, Amemiya S, Katow H (2000) Initial analysis of immunochemical cell surface properties, location and formation of the serotonergic apical ganglion in sea urchin embryos. Dev Growth Differ 42:479–488
Zigler KS, Raff EC, Popodi E, Raff RA, Lessios HA (2003) Adaptive evolution of bindin in the genus Heliocidaris is correlated with the shift to direct development. Evolution 57:2293–2302
Acknowledgments
We thank H. Abe, Research Center for Marine Biology, Tohoku University for raising older larvae of the sea urchin for this study. This work was supported by a grant from the Australian Research Council. We also thank Dr. V. Morris, Biological Science, University of Sydney for valuable discussion for this study.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by N. Satoh
Rights and permissions
About this article
Cite this article
Katow, H., Elia, L. & Byrne, M. Development of nervous systems to metamorphosis in feeding and non-feeding echinoid larvae, the transition from bilateral to radial symmetry. Dev Genes Evol 219, 67–77 (2009). https://doi.org/10.1007/s00427-008-0266-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00427-008-0266-4