Skip to main content
SpringerLink
Log in

Heterochronies in the formation of the nervous and digestive systems in early postlarval development of opisthobranch mollusks: Organization of major organ systems of the arctic dorid Cadlina laevis

  • Conference Materials
  • Published:
Biology Bulletin Aims and scope Submit manuscript

Abstract

For the first time using laser confocal microscopy and histochemical and immunocytochemical methods (detection of F-actine, catecholamines, acetylcholintransferase, substance P and FMRFamide) in combination with classical histological methods and electron microscopy of whole-mount preparations, the structure and patterns of formation of the nervous, muscular, and digestive systems in early postlarval development (from 2 days to 4 months) in the opisthobranch mollusk Cadlina laevis were studied. Heterochronies manifested in positive allometry of the sensory organs, ganglia of the central nervous system, and the pharyngeal region of the digestive system in relation to overall body size in juvenile specimens compared to adult animals were detected.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Barbour, M.A., Note on the distribution and food preference of Cadlina laevis (Nudibranchia: Chromodoridae), Nautilus, 1979, vol. 93, nos. 2–3, pp. 61–62.

    Google Scholar 

  • Bickell, L. and Kempf, S., Larval and metamorphic morphogenesis in the nudibranch Melibe leonine (Mollusca: Opisthobranchia), Biol. Bull., 1983, vol. 165, pp. 119–138.

    Article  Google Scholar 

  • Boyd, P.J., Osborne, N.N., and Walker, R.J., Localization of a substance P-like material in the central and peripheral nervous system of the snail Helix aspersa, Histochemistry, 1986, vol. 84, no. 1, pp. 97–103.

    Article  CAS  PubMed  Google Scholar 

  • Bullock, T.H. and Horridge, G.A., Structure and Function in the Nervous System of Invertebrates, San Francisco: Calif.: W.H. Freeman, 1965.

    Google Scholar 

  • Carroll, S.B., Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution, Cell, 2008, vol. 134, pp. 25–36.

    Article  CAS  PubMed  Google Scholar 

  • Chase, R., Lessons from snail tentacles, Chem. Senses, 1986, vol. 11, no. 4, pp. 411–426.

    Article  Google Scholar 

  • Croll, R.P., Catecholamine-containing cells in the central nervous system and periphery of Aplysia californica, J. Comp. Neurol., 2001, vol. 441, no. 2, pp. 91–105.

    Article  CAS  PubMed  Google Scholar 

  • Croll, R.P. and Voronezhskaya, E.E., Early FMRFamidelike immunoreactive cells in gastropod neurogenesis, Acta Biol. Hung., 1995, vol. 46, nos. 2–4, pp. 295–303.

    CAS  PubMed  Google Scholar 

  • Croll, R.P., Voronezhskaya, E.E., Hiripi, L., and Elekes, K., Development of catecholaminergic neurons in the pond snail, Lymnaea stagnalis: II. postembryonic development of central and peripheral cells, J. Comp. Neurol., 1999, vol. 404, no. 3, pp. 297–309.

    Article  CAS  PubMed  Google Scholar 

  • Fominykh, M.Ya., Sensitive nerve cells in the epithelium and subepithelial connective tissue of trunk segments of polychaetes Nephthys hombergii and Harmathoe imbricate, Zh. Evol. Biokhim. Fiziol., 1982, vol. 18, no. 52, pp. 507–513.

    Google Scholar 

  • Furness, J.B., Costa, M., and Wilson, A.J., Water-stable fluorophores, produced by reaction with aldehyde solutions, for the histochemical localization of catechol- and indolethylamines, Histochemistry, 1977, vol. 52, no. 2, pp. 159–170.

    Article  CAS  PubMed  Google Scholar 

  • Hernádi, L. and Elekes, K., Topographic organization of serotonergic and dopaminergic neurons in the cerebral ganglia and their peripheral projection patterns in the head areas of the snail Helix pomatia, J. Comp. Neurol., 1999, vol. 411, no. 2, pp. 274–287.

    Article  PubMed  Google Scholar 

  • Kempf, S.C., Chun, G.V., and Hadfield, M.G., An immunocytochemical search for potential neurotransmitters in larvae of Phestilla sibogae (Gastropoda, Opisthobranchia), Comp. Biochem. Physiol. Pt C: Comp. Pharmacol., 1992, vol. 101, no. 2, pp. 299–305.

    Article  Google Scholar 

  • Kononenko, N.L. and Zhukov, V.V., Neuroanatomical and immunocytochemical studies of the head retractor muscle innervation in the pond snail, Lymnaea stagnalis L., Zoology (Jena), 2005, vol. 108, no. 3, pp. 217–237.

    Article  CAS  PubMed  Google Scholar 

  • Kristof, A. and Klussmann-Kolb, A., Neuromuscular development of Aeolidiella stephanieae Valdez, 2005 (Mollusca, Gastropoda, Nudibranchia), Front. Zool., 2010, vol. 7, no. 10, p. 5.

    Article  PubMed Central  PubMed  Google Scholar 

  • Lehman, H.K. and Price, D.A., Localization of FMRFamidelike peptides in the snail Helix aspersa, J. Exp. Biol., 1987, vol. 131, pp. 37–53.

    CAS  PubMed  Google Scholar 

  • Lloyd, P.E. and Church, P.J., Cholinergic neuromuscular synapses in Aplysia have low endogenous acetylcholinesterase activity and a high-affinity uptake system for acetylcholine, J. Neurosci., 1994, vol. 14, no. 11, pt 1, pp. 6722–6733.

    CAS  PubMed  Google Scholar 

  • Marois, R. and Carew, T.J., The gastropod nervous system in metamorphosis, J. Neurobiol., 1990, vol. 21, no. 7, pp. 1053–1071.

    Article  CAS  PubMed  Google Scholar 

  • Martynov, A.V. and Schröbl, M., Phylogeny and evolution of corambid nudibranchs (Mollusca: Gastropoda), Zool. J. Linn. Soc., 2011, vol. 163, pp. 585–604.

    Article  Google Scholar 

  • Martynov, A.V., From “tree-thinking” to “cycle-thinking”: ontogenetic systematics of nudibranch molluscs, Thalassas, 2011, vol. 27, pp. 193–224.

    Google Scholar 

  • Martynov, A.V., Ontogenetic systematics: the synthesis of taxonomy, phylogenetics, and evolutionary developmental biology, Paleontol. J., 2012, vol. 46, pp. 833–864.

    Article  Google Scholar 

  • Moroz, L., Nezlin, L., Elofsson, R., and Sakharov, D., Serotonin-and FMRFamide-immunoreactive nerve elements in the chiton Lepidopleurus asellus (Mollusca, Polyplacophora), Cell Tiss. Res., 1994, vol. 275, no. 2, pp. 277–282.

    Article  Google Scholar 

  • Ovsyannikov, V.I., Neiromediatory i gormony v zheludochnokishechnom trakte (integrativnye aspekty) (Neurotransmitters and Hormones in the Gastrointestinal Tract (Integrative Aspects)), St. Petersburg, 2003.

    Google Scholar 

  • Perron, F.E. and Turner, R.D., Development, metamorphosis, and natural history of the nudibranch Doridella obscura Verrill (Corambidae: Opisthobranchia), J. Exp. Mar. Bio. Ecol., 1977, vol. 27, no. 2, pp. 171–185.

    Article  Google Scholar 

  • Punin, M.Yu., Kishechnaya regulyatornaya sistema bespozvonochnykh zhivotnykh i ee predpolagaemaya evolyutsiya u mnogokletochnykh (Intestinal Regulatory System of Invertebrates and Its Presumable Evolution in Metazoans), Tr. ZIN RAN, 2001, vol. 290.

  • Quinlan, E.M., Arnett, B.C., and Murphy, A.D., Feeding stimulants activate an identified dopaminergic interneuron that induces the feeding motor program in Helisoma, J. Neurophysiol., 1997, vol. 78, no. 2, pp. 812–824.

    CAS  PubMed  Google Scholar 

  • Romeis, B., Mikroskopische, Technik, Munchen: Leibniz-Verlag, 1948.

    Google Scholar 

  • Romeis, B., Mikroskopicheskaya tekhnika (Microscopic Techniques), Sokolov, I.I., Ed., Moscow: Izd. Inostr. Lit., 1953.

  • Schot, L.P., Boer, H.H., Swaab, D.F., and Van Noorden, S., Immunocytochemical demonstration of peptidergic neurons in the central nervous system of the pond snail Lymnaea stagnalis with antisera raised to biologically active peptides of vertebrates, Cell Tiss. Res., 1981, vol. 216, no. 2, pp. 273–291.

    Article  CAS  Google Scholar 

  • Suzuki, H., Kimura, T., Sekiguchi, T., and Mizukami, A., FMRF amide-like-immunoreactive primary sensory neurons in the olfactory system of the terrestrial mollusc, Limax marginatus, Cell Tiss. Res., 1997, vol. 289, no. 2, pp. 339–345.

    Article  CAS  Google Scholar 

  • Thompson, T.E., Direct development in a nudibranch, Cadlina laevis, with a discussion of developmental processes in Opisthobranchia, J. Mar. Biol. Assoc. Unit. Kingdom, 1967, vol. 47, no. 1, pp. 1–22.

    Article  Google Scholar 

  • De la Torre, J.C. and Surgeon, J.W., A methodological approach to rapid and sensitive monoamine histofluorescence using a modified glyoxylic acid technique: the SPG method, Histochemistry, 1976, vol. 49, no. 2, pp. 81–93.

    Article  CAS  PubMed  Google Scholar 

  • Voronezhskaya, E.E., Hiripi, L., Elekes, K., and Croll, R.P., Development of catecholaminergic neurons in the pond snail, Lymnaea stagnalis: I. Embryonic development of dopamine-containing neurons and dopamine-dependent behaviors, J. Comp. Neurol., 1999, vol. 404, no. 3, pp. 285–296.

    Article  CAS  PubMed  Google Scholar 

  • Wägele, H., Klussmann-Kolb, A., Verbeek, E., and Schröbl, M., Flashback and foreshadowing—a review of the taxon Opisthobranchia, Org. Divers. Evol., 2013, vol. 14, no. 1, pp. 133–149.

    Article  Google Scholar 

  • Wanninger, A., Comparative lophotrochozoan neurogenesis and larval neuroanatomy: recent advances from previously neglected taxa, Acta Biol. Hung., 2008, vol. 59(suppl.), pp. 127–136.

    Article  PubMed  Google Scholar 

  • Wanninger, A., Shaping the things to come: ontogeny of lophotrochozoan neuromuscular systems and the tetraneuralia concept, Biol. Bull., 2009, vol. 216, no. 3, pp. 293–306.

    PubMed  Google Scholar 

  • Webster, M. and Zelditch, M.L., Evolutionary modifications of ontogeny: heterochrony and beyond, Paleobiology, 2005, vol. 31, pp. 354–372.

    Article  Google Scholar 

  • Wollesen, T., Wanninger, A., and Klussmann-Kolb, A., Neurogenesis of cephalic sensory organs of Aplysia californica, Cell Tiss. Res., 2007, vol. 330, no. 2, pp. 361–379.

    Article  Google Scholar 

  • Wollesen, T., Wanninger, A., and Klussmann-Kolb, A., Myogenesis in Aplysia californica (Cooper, 1863) (Mollusca, Gastropoda, Opisthobranchia) with special focus on muscular remodeling during metamorphosis, J. Morphol., 2008, vol. 269, no. 7, pp. 776–789.

    Article  PubMed  Google Scholar 

  • Wyeth, R.C. and Croll, R.P., Peripheral sensory cells in the cephalic sensory organs of Lymnaea stagnalis, J. Comp. Neurol., 2011, vol. 519, no. 10, pp. 1894–1913.

    Article  PubMed  Google Scholar 

  • Yablokov, A.V. and Yusufov, A.G., Evolyutsionnoe uchenie (Evolutionary Theory), Moscow: Vyssh. Shk., 1976.

    Google Scholar 

  • Zaitseva, O.V., Characteristics of the neuronal composition of the central nervous system of nudibranch mollusks, Zh. Evol. Biokhim. Fiziol., 1978, vol. 14, no. 5, pp. 497–503.

    CAS  PubMed  Google Scholar 

  • Zaitseva, O.V., Structural organization receptor elements and organs of the land mollusks Pomatias elegans (Prosobranchia), Neurosci. Behav. Physiol., 1997, vol. 27, no. 5, pp. 533–540.

    Article  CAS  PubMed  Google Scholar 

  • Zaitseva, O.V., The structural organization of the sensory system of statocysts of nudibranchs and characteristics of intersensory interactions, Morfologiya, 1999, vol. 115, no. 6, pp. 26–32.

    Google Scholar 

  • Zaitseva, O.V., Dominant structural and functional adaptations of distant chemosensory systems in phylogenesis of Gastropoda, Ross. Fiziol. Zh. im. I.M. Sechenova, 2000a, vol. 86, no. 8, pp. 995–1006.

    CAS  PubMed  Google Scholar 

  • Zaitseva, O.V., Projection connections and a hypothetical scheme of the structural organization of the procerebrum of terrestrial mollusks, Zh. Evol. Biokhim. Fiziol., 2000b, vol. 36, no. 5, pp. 470–483.

    Google Scholar 

  • Zaitseva, O.V., Morphological characteristic of ommatophore olfactory organs in gastropod mollusks (principle of evolutionary parallelism), Proc. Zool. Inst. Russ. Acad. Sci., St. Petersburg, 2002, vol. 296, pp. 171–176.

    Google Scholar 

  • Zaitseva, O.V., Comparative study of nervous elements and their interaction with the endocrine glands and the muscle retractors in the ommatophores of snails and slugs, Zh. Evol. Biokhim. Fiziol., 2004, vol. 40, no. 6, pp. 556–568.

    CAS  PubMed  Google Scholar 

  • Zaitseva, O.V. and Bocharova, L.S., Sensory cells in the head skin of pond snails. Fine structure of sensory endings, Cell Tiss. Res., 1981, vol. 220, no. 4, pp. 797–807.

    Article  Google Scholar 

  • Zaitseva, O.V. and Kuznetsova, T.V., Distribution of acetylcholinesterase activity in the digestive system of the gastropod molluscs Littorina littorea and Achatina fulica, Morfologiya, 2008, vol. 133, no. 1, pp. 55–59.

    CAS  Google Scholar 

  • Zaitseva, O.V. and Markosova, T.G., Acetylcholine, nitric oxide and their possible colocalization in regulatory cells of the digestive system of gastropods, Dokl. Ross. Akad. Nauk, 2008, vol. 421, no. 1, pp. 248–250.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg, 199034, Russia

    O. V. Zaitseva & A. N. Shumeev

  2. Koltzov Institute of Developmental Biology RAS, ul. Vavilova 26, Moscow, 119334, Russia

    T. A. Korshunova

  3. Zoological Museum of Moscow State University, ul. Bol’shaya Nikitskaya 6, Moscow, 125009, Russia

    A. V. Martynov

Authors
  1. O. V. Zaitseva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. N. Shumeev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. A. Korshunova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. V. Martynov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to O. V. Zaitseva.

Additional information

Original Russian Text © O.V. Zaitseva, A.N. Shumeev, T.A. Korshunova, A.V. Martynov, 2015, published in Izvestiya Akademii Nauk, Seriya Biologicheskaya, 2015, No. 3, pp. 237–247.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zaitseva, O.V., Shumeev, A.N., Korshunova, T.A. et al. Heterochronies in the formation of the nervous and digestive systems in early postlarval development of opisthobranch mollusks: Organization of major organ systems of the arctic dorid Cadlina laevis . Biol Bull Russ Acad Sci 42, 186–195 (2015). https://doi.org/10.1134/S1062359015030152

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062359015030152

Keywords

Search

Navigation