Abstract
The morphogenesis of serotonin- and FMRF-amide-bearing neuronal elements in the scaphopod Antalis entalis was investigated by means of antibody staining and confocal laser scanning microscopy. Nervous system development starts with the establishment of two initial, flask-like, serotonergic central cells of the larval apical organ. Slightly later, the apical organ contains four serotonergic central cells which are interconnected with two lateral serotonergic cells via lateral nerve projections. At the same time the anlage of the adult FMRF-amide-positive cerebral nervous system starts at the base of the apical organ. Subsequently, the entire neuronal complex migrates behind the prototroch and the six larval serotonergic cells lose transmitter expression prior to metamorphic competence. There are no strictly larval FMRF-amide-positive neuronal structures. The development of major adult FMRF-amide-containing components such as the cerebral system, the visceral loop, and the buccal nerve cords, however, starts before the onset of metamorphosis. The anlage of the putative cerebral system is the only site of adult serotonin expression in Antalis larvae. Establishment of the adult FMRF-amidergic and serotonergic neuronal bauplan proceeds rapidly after metamorphosis. Neurogenesis reflects the general observation that the larval phase and the expression of distinct larval morphological features are less pronounced in Scaphopoda than in Gastropoda or Bivalvia. The degeneration of the entire larval apical organ before metamorphic competence argues against an involvement of this sensory system in scaphopod metamorphosis. The lack of data on the neurogenesis in the aplacophoran taxa prevent a final conclusion regarding the plesiomorphic condition in the Mollusca. Nevertheless, the results presented herein shed doubts on general theories regarding possible functions of larval "apical organs" of Lophotrochozoa or even Metazoa.
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References
Beer A-J, 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 200:268–280
Boore JL, Staton JL (2002) The mitochondrial genome of the sipunculid Phascolopsis gouldii supports its association with Annelida rather than Mollusca. Mol Biol Evol 19:127–137
Chaffe C, Lindberg DR (1986) Larval biology of early Cambrian molluscs: the implications of small body size. Bull Mar Sci 39:536–549
Chia F-S, Koss R (1984) Fine structure of the cephalic sensory organ in the larva of the nudibranch Rostanga pulchra (Mollusca, Opisthobranchia, Nudibranchia). Zoomorphology 104:131–139
Cragg SM, Crisp M (1991) The biology of scallop larvae. In: Shumway SE (ed) Biology, ecology and aquaculture of scallops. Elsevier, Amsterdam, pp 75–132
Croll RP (2000) Insights into early molluscan neuronal development through studies of transmitter phenotypes in embryonic pond snails. Microsc Res Tech 49:570–578
Croll RP, Jackson DL, Voronezhskaya EE (1997) Catecholamine-containing cells in larval and postlarval bivalve molluscs. Biol Bull 193:116–124
Dickinson AJG, Nason J, Croll RP (1999) Histochemical localization of FMRF-amide, serotonin and catecholamines in embryonic Crepidula fornicata (Gastropoda, Prosobranchia). Zoomorphology 119:49–62
Dickinson AJG, Croll RP, Voronezhskaya EE (2000) Development of embryonic cells containing serotonin, catecholamines, and FMRF-amide-related peptides in Aplysia californica. Biol Bull 199:305–315
Diefenbach TJ, Koss R, Goldberg JI (1998) Early development of an identified serotonergic neuron in Helisoma trivolvis embryos: serotonin expression, de-expression, and uptake. J Neurobiol 34:361–376
Friedrich S, Wanninger A, Brückner M, Haszprunar G (2002) Neurogenesis in the mossy chiton, Mopalia muscosa (Gould) (Polyplacophora): evidence against molluscan metamerism. J Morphol 253:109–117
Goldberg JI, Kater SB (1989) Expression and function of the neurotransmitter serotonin during development of the Helisoma nervous system. Dev Biol 131:483–495
Haszprunar G (2000) Is the Aplacophora monophyletic? A cladistic point of view. Am Malac Bull 15:115–130
Haszprunar G, Salvini-Plawen Lv, Rieger RM (1995) Larval planktotrophy: a primitive trait in the Bilateria? Acta Zool (Stockh) 76:141–154
Haszprunar G, Friedrich S, Wanninger A, Ruthensteiner B (2002) Fine structure and immunocytochemistry of a new chemosensory system in the chiton larva (Mollusca: Polyplacophora). J Morphol 252:210–218
Hay-Schmidt A (2000) The evolution of the serotonergic nervous system. Proc R Soc Lond B 267:1071–1079
Ierusalimsky VN, Balaban PM (2001) Ontogenesis of the snail, Helix aspersa: embryogenesis timetable and ontogenesis of GABA-like immunoreactive neurons in the central nervous system. J Neurocytol 30:73–91
Kempf SC, Page LR, Pires A (1997) Development of serotonin-like immunoreactivity in the embryos and larvae of nudibranch molluscs with emphasis on the structure and possible function of the apical sensory organ. J Comp Neurol 386:507–528
Kowalevsky MA (1883) Etude sur l'embryogénie du Dentale. Ann Mus Hist Nat Marseille 1:5–46, pls 1–8
Lacalli TC, Kelly SJ (2002) Anterior neural centres in echinoderm bipinnaria and auricularia larvae: cell types and organization. Acta Zool (Stockh) 83:99–110
Lacaze-Duthiers H (1857) Histoire de l'organisation et du développement du Dentale. Ann Sci Nat Zool 7:171–255, pls 5–9
Lin MF, Leise EM (1996) Gangliogenesis in the prosobranch gastropod Ilyanassa obsoleta. J Comp Neurol 374:180–193
Marois R, Carew TJ (1997a) Ontogeny of serotonergic neurons in Aplysia californica. J Comp Neurol 386:477–490
Marois R, Carew TJ (1997b) Projection patterns and target tissues of the serotonergic cells in larval Aplysia californica. J Comp Neurol 386:491–506
Marois R, Carew TJ (1997c) Fine structure of the apical ganglion and its serotonergic cells in the larva of Aplysia californica. Biol Bull 192:388–398
Marois R, Croll RP (1992) Development of serotoninlike immunoreactivity in the embryonic nervous system of the snail Lymnaea stagnalis. J Comp Neurol 322:255–265
Page LR (2002) Apical sensory organ in larvae of the patellogastropod Tectura scutum. Biol Bull 202:6–22
Page LR, Parries SC (2000) Comparative study of the apical ganglion in planktotrophic caenogastropod larvae: ultrastructure and immunoreactivity to serotonin. J Comp Neurol 418:383–401
Raineri M (1995) Is a mollusc an evolved bent metatrochophore? A histochemical investigation of neurogenesis in Mytilus (Mollusca: Bivalvia). J Mar Biol Assoc UK 75:571–592
Runnegar B, Pojeta J Jr (1974) Molluscan phylogeny: the paleontological viewpoint. Science 186:311–317
Salvini-Plawen Lv, Steiner G (1996) Synapomorphies and plesiomorphies in higher classification of Mollusca. In: Taylor JD (ed) Origin and evolutionary radiation of the Mollusca. Oxford University Press, Oxford, pp 29–51
Santagata S (2002) Structure and metamorphic remodeling of the larval nervous system and musculature of Phoronis pallida (Phoronida). Evol Dev 4:28–42
Shigeno S, Kidokoro H, Goto T, Tsuchiya K, Segawa S (2001a) Early ontogeny of the Japanese common squid Todarodes pacificus (Cephalopoda, Ommastrephidae) with special reference to its characteristic morphology and ecological significance. Zool Sci 18:1011–1026
Shigeno S, Kidokoro H, Tsuchiya K, Segawa S, Yamamoto M (2001b) Development of the brain in the oegopsid squid Todarodes pacificus: an atlas up to the hatching stage. Zool Sci 18:527–541
Shigeno S, Tsuchiya K, Segawa S (2001c) Embryonic and paralarval development of the central nervous system of the loliginid squid Sepioteuthis lessoniana. J Comp Neurol 437:449–475
Shimek RL, Steiner G (1997) Scaphopoda. In: Harrison FW, Kohn AJ (eds) Microscopic anatomy of invertebrates, vol 6B. Mollusca II. Wiley-Liss, New York, pp 719–718
Smith SA, Nason J, Croll RP (1998) Distribution of catecholamines in the sea scallop, Placopecten magellanicus. Can J Zool 76:1254–1262
Steiner G, Dreyer H (2002) Cephalopoda and Scaphopoda are sister taxa: an evolutionary scenario. Zoology 105(suppl V):95
Tardy J, Dongard S (1993) Le complexe apical de la véligère de Ruditapes philippinarium (Adams and Reeve, 1850) (Mollusque, Bivalve, Vénèridé). C R Acad Sci 316:177–184
Voronezhskaya EE, Elekes K (1993) Distribution of serotonin-like immunoreactive neurones in the embryonic nervous system of lymnaeid and planorbid snails. Neurobiology 1:371–383
Voronezhskaya EE, Tyurin SA, Nezlin LP (2002) Neuronal development in larval chiton Ischnochiton hokadodensis (Mollusca, Polyplacophora). J Comp Neurol 444:25–38
Waller TR (1998) Origin of the molluscan class Bivalvia and a phylogeny of major groups. In: Johnston PA, Haggart JW (eds) Bivalves: an eon of evolution. University of Calgary Press, Calgary, pp 1–45
Wanninger A, Haszprunar G (2001) The expression of an engrailed protein during embryonic shell formation of the tusk-shell, Antalis entalis (Mollusca, Scaphopoda). Evol Dev 3:312–321
Wanninger A, Haszprunar G (2002) Muscle development in Antalis entalis (Mollusca, Scaphopoda) and its significance for scaphopod relationships. J Morphol 254:53–64
Zardus JD, Morse MP (1998) Embryogenesis, morphology and ultrastructure of the pericalymma larva of Acila castrensis (Bivalvia: Protobranchia: Nuculoida). Invertebr Biol 117:221–244
Acknowledgements
We thank Dr. G. Steiner (Vienna) for species identification, Prof. Dr. C.N. David and Dr. O. Alexandrova (both Department of Biology II, Munich) for providing confocal facilities, and S. Santagata (Los Angeles) for methodological advice. The financial support of the Deutsche Forschungsgemeinschaft (DFG) is gratefully acknowledged (grants WA 1580/1–1 and HA 2598/1–3, 1–4).
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Wanninger, A., Haszprunar, G. The development of the serotonergic and FMRF-amidergic nervous system in Antalis entalis (Mollusca, Scaphopoda). Zoomorphology 122, 77–85 (2003). https://doi.org/10.1007/s00435-003-0071-6
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DOI: https://doi.org/10.1007/s00435-003-0071-6