Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-22T18:23:06.650Z Has data issue: false hasContentIssue false
  • English
  • Français

Is a mollusc an evolved bent metatrochophore? A histochemical investigation of neurogenesis in Mytilus (Mollusca: Bivalvia)

Published online by Cambridge University Press:  11 May 2009

Margherita Raineri
Margherita Raineri
Affiliation:
Institute of Comparative Anatomy, University of Genoa, Vie Benedetto XV, 5, 16132 Genoa, Italy
Get access Rights & Permissions [Opens in a new window]

Extract

Acetylcholinesterase (AChE) activity, a marker of neural differentiation, was histo-chemically localized in embryos and larvae of Mytilus galloprovincialis Lamarck and M. edulis L. (Mollusca: Bivalvia). The results show that: (1) the first AChE-active cells develop as two bilaterally symmetrical, postero-dorsal pioneer sensory neurons and their supporting superficial cells; (2) the pathways of their pioneering longitudinal axons are the same as those of two bilaterally symmetrical nerve cords which differentiate later in a postero-anterior direction; (3) in the conchostoma larva the posterior neurons and their associated superficial AChE-active cells give rise to two ciliary sensory-like organs which are the earliest rudiments of pedal ganglia and primary byssus glands; (4) three pairs of posttrochal gangliar rudiments, most probably visceral, parietal and pleural ganglia, develop on the same longitudinal nerve cords in the trochophore larva; (5) starting from the veliger stage, the presumptive foot rotates on the ventral side and migrates forwards, so that this gangliar chain is bent and the viscero-parietal ganglia become localized dorso-posteriorly to the pedal ganglia; (6) the cerebral ganglia differentiate together with the apical organ and the nerve network of the velum after the first pedal nerve rudiments have been detected.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 75 , Issue 3 , August 1995 , pp. 571 - 592
Copyright
Copyright © Marine Biological Association of the United Kingdom 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Åkesson, B., 1966. On the nervous system of the Lopadorhynchus larva (Polychaeta). Arkiv för Zoologi, 20, 55–78.Google Scholar
Ansell, A.D., 1962. The functional morphology of the larva, and the post-larval development of Venus striatula (Da Costa). Journal of the Marine Biological Association of the United Kingdom, 42, 419–443.CrossRefGoogle Scholar
Bayne, B.L., 1976. The biology of mussel larvae. In Marine mussels: their ecology and physiology (ed. B.L., Bayne), pp. 81–120. Cambridge University Press.Google Scholar
Beklemishev, V.N., 1969. Principles of promorphology of Trochozoa. In Principles of comparative anatomy of invertebrates, vol. 1 (ed. Z., Kabata), pp. 139–187. Edinburgh: Oliver & Boyd. [Translated from Russian.]Google Scholar
Bülbring, E., Burn, J.H. & Shelley, H.J., 1953. Acetylcholine and ciliary movement in the gill plates of Mytilus edulis. Proceedings of the Royal Society B, 141, 445–466.Google Scholar
Cragg, S.M. & Nott, J.A., 1977. The ultrastructure of the statocysts in the pediveliger larvae of Pecten maximus (L.) (Bivalvia). Journal of Experimental Marine Biology and Ecology, 27, 23–36.CrossRefGoogle Scholar
Cranfield, H.J., 1973. A study of the morphology, ultrastructure, and histochemistry of the foot of the pediveliger of Ostrea edulis. Marine Biology, 22, 187–202.CrossRefGoogle Scholar
Dawydoff, C., 1928. Traité d'embryologie comparée des invertébrés. Paris: Masson & Cie.Google Scholar
Dorresteijn, A.W.C., 1990. Quantitative analysis of cellular differentiation during early embryo-genesis of Platynereis dumerilü. Wilhelm Roux's Archives of Developmental Biology, 199, 14–30.Google Scholar
Dorresteijn, A.W.C. & Graffy, C., 1993. Competence of blastomeres for the expression of molecular tissue markers is acquired by diverse mechanisms in the embryo of Platynereis (Annelida). Wilhelm Roux's Archives of Developmental Biology, 202, 270–275.CrossRefGoogle Scholar
Dorresteijn, A.W.C., O'grady, B., Fischer, A., Porchet-Henneré, E. & Boilly-Marer, Y., 1993. Molecular specification of cell lines in the embryo of Platynereis (Annelida). Wilhelm Roux's Archives of Developmental Biology, 202, 260–269.CrossRefGoogle Scholar
Drews, U., 1975. Cholinesterase in embryonic development. Progress in Histochemistry and Cyto-chemistry, 7, 1–52.Google Scholar
Falugi, C., 1993. Localization and possible role of molecules associated with the cholinergic system during ‘non-nervous’ developmental events. European Journal of Histochemistry, 37, 287–294.Google ScholarPubMed
Falugi, C. & Davoli, C., 1993. Localization of putative biochemical messengers during Eisenia foetida (Annelida, Oligochaeta) development. l'issue and Cell, 25, 311–323.Google ScholarPubMed
Gilloteaux, J., 1978. Innervation du muscle rétracteur antérieur du byssus (ABRM) de Mytilus edulis L. et de Mytilus galloprovincialis Lmk. Histochemistry, 55, 209–224.Google Scholar
Gruffydd, L.D., Lane, D.J.W. & Beaumont, A.R., 1975. The glands of the larval foot in Pecten maximus L. and possible homologues in other bivalves. Journal of the Marine Biological Association of the United Kingdom, 55, 463–476.Google Scholar
Haeckel, E., 1874. Die Gastraea-Theorie, die phylogenetische Classification des Tierreichs und die Homologie der Keimblätter. Zeitschrift für Naturwissenschaft, Jena, 9, 402–508.Google Scholar
Hasseigaku, M.D., 1968. Mollusca. In Invertebrate embryology (ed. M., Kumé and K., Dan), pp. 485–525. Belgrade: NOLIT Publishing House.Google Scholar
Hatschek, B., 1878. Studien über Entwicklungsgeschichte der Anneliden. Ein Beitrag zur Morpholgie der Bilaterien. Arbeiten aus den Zoologischen Institute der Universität Wien und der Zoologischen Station in Triest, 1, 277–404.Google Scholar
Hatschek, B., 1880. Entwicklungsgeschichte von Teredo. Arbeiten aus den Zoologischen Institute der Universität Wien und der Zoologischen Station in Triest, 3, 1–44.Google Scholar
Hatschek, B., 1888. Lehrbuch der Zoologie. Eine Morphologische Übersicht des Thierreiches zur Einführung in das Studium dieser Wissenschaft. Jena: Verlag von Gustav Fisher.CrossRefGoogle Scholar
Karnovsky, M.J. & Roots, L., 1964. A ‘direct coloring’ thiocholine method for cholinesterases. Journal of Histochemistry and Cytochemistry, 12, 219–221.CrossRefGoogle ScholarPubMed
Klose, M. & Bentley, D., 1989. Transient pioneer neurons are essential for formation of an embryonic peripheral nerve. Science, New York, 245, 982–984.Google Scholar
Lane, D.J.W & Nott, J.A., 1975. A study of the morphology, fine structure and histochemistry of the foot of the pediveliger of Mytilus edulis L. Journal of the Marine Biological Association of the United Kingdom, 55, 477–495.CrossRefGoogle Scholar
Longo, F.J. & Anderson, E., 1969a. Cytological aspects of fertilization in the lamellibranch, Mytilus edulis. I. Polar body formation and development of the female pronucleus. Journal of Experi-mental Zoology, 172, 69–96.CrossRefGoogle ScholarPubMed
Longo, F.J. & Anderson, E., 1969b. Cytological aspects of fertilization in the lamellibranch, Mytilus edulis. II. Development of the male pronucleus and the association of the maternally and paternally derived chromosomes. Journal of Experimental Zoology, 172, 97–119.CrossRefGoogle ScholarPubMed
Malakhov, V.V. & Medvedeva, L.A., 1985. Embryonic and early larval development in the bivalve Mytilus edulis (Mytilida, Mytilidae). Zoologhiceskiî Zhurnal, 64, 1808–1815. [In Russian with English summary.]Google Scholar
McLaren, D.J., 1976. Sense organs and their secretions. In The organization of nematodes (ed. N.A., Croll), pp. 139–161. London: Academic Press.Google Scholar
Meisenheimer, J., 1901. Entwicklungsgeschichte von Dreissensia polymorpha Pall. Zeitschrift für Wissenschaftlichte Zoologie, 69, 1–137.Google Scholar
Moor, B., 1982. A transitory structure in early organogenesis of the nervous system in Stylommatophora (Gastropoda Pulmonata). Malacologia, 22, 611–614.Google Scholar
Moor, B., 1983. Organogenesis. In The Mollusca, vol. 3 (ed. N.H., Verdonk and J.A.M., Van Den Biggelaar), pp. 49–177. New York: Academic Press.Google Scholar
Nielsen, C., 1985. Animal phylogeny in the light of the trochaea theory. Biological Journal of the Linnean Society, 25, 243–299.CrossRefGoogle Scholar
Ospovat, M.F., Kulakovski, E.E. & Flyatchinskaya, L.P., 1989. Some aspects of revealing mediator systems in early mussels (Mytilus edulis L.) ontogenesis. Proceedings of the Zoological Institute, Leningrad, USSR Academy of Sciences, 203, 76–83. [In Russian.]Google Scholar
Raineri, M., 1984. Histochemical investigations of Rotifera Bdelloidea. I. Localization of cholinesterase activity. Histochemical Journal, 16, 601–616.Google Scholar
Raineri, M., 1989. Enzyme markers in development: cholinesterase (ChE), acid hydrolases, alkaline phosphatase (ALP) and aminopeptidase (AP) in embryos and larvae of Artemia. In Cell and molecular biology of Artemia development (ed. A.H., Warner et al.), pp. 131–156. New York: Plenum Press. [NATO ASI Series A, vol. 174.]CrossRefGoogle Scholar
Raineri, M. & Falugi, C., 1983. Acetylcholinesterase activity in embryonic and larval development of Artemia salina Leach (Crustacea Phyllopoda). Journal of Experimental Zoology, 227, 229–246.Google Scholar
Raineri, M. & Ospovat, M., 1994. The initial development of gangliar rudiments in a posterior position in Mytilus galloprovincialis (Mollusca: Bivalvia). Journal of the Marine Biological Association of the United Kingdom, 74, 73–77.Google Scholar
Rattenbury, J.C. & Berg, W.E., 1954. Embryonic segregation during early development of Mytilus edulis. Journal of Morphology, 95, 393–414.CrossRefGoogle Scholar
Raven, C.P., 1958. Morphogenesis: the analysis of molluscan development. London: Pergamon Press.Google Scholar
Seaman, G.R. & Houlihan, R.K., 1951. Enzyme systems in Tetrahymena geleii S. II. Acetylcholinesterase activity. Its relation to motility of the organism and to coordinated ciliary action in general. Journal of Cellular and Comparative Physiology, 37, 309–321.Google Scholar
Thomas, J.B., Bastiani, M.J., Bate, M. & Goodman, C.S., 1984. From grasshopper to Drosophila: a common plan for neuronal development. Nature, London, 310, 203–207.Google Scholar
Verdonk, N.H. & Biggelaar, J.A.M. Van Den, 1983. Early development and the formation of the germ layers. In The Mollusca, vol. 3 (ed. N.H., Verdonk and J.A.M., Van Den Biggelaar), pp. 91–122. New York: Academic Press.Google Scholar
Willmer, P., 1990. Invertebrate relationships. Patterns in animal evolution. Cambridge University Press.CrossRefGoogle Scholar
Ziegler, H.E., 1885. Die Entwicklung von Cyclas cornea Lam. (Sphaerium corneum L.). Zeitschrift für Wissenschaftliche Zoologie, 41, 525–569.Google Scholar