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The phylogeny of invertebrates and the evolution of myelin

Published online by Cambridge University Press:  10 June 2009

Betty I. Roots*
Affiliation:
Department of Cell and Systems Biology, University of Toronto, Toronto, Ontario, Canada
*
Correspondence should be addressed to: Betty I. Roots, Department of Cell and Systems Biology, University of Toronto, 25 Harbord Street, Toronto, Ontario M5S 3G5, Canada phone: 416 486 9950 e-mail: [email protected]

Abstract

Current concepts of invertebrate phylogeny are reviewed. Annelida and Arthropoda, previously regarded as closely related, are now placed in separate clades. Myelin, a sheath of multiple layers of membranes around nerve axons, is found in members of the Annelida, Arthropoda and Chordata. The structure, composition and function of the sheaths in Annelida and Arthropoda are examined and evidence for the separate evolutionary origins of myelin in the three clades is presented. That myelin has arisen independently at least three times, namely in Annelids, Arthropodas and Chordates, provides a remarkable example of convergent evolution.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Aguinaldo, A.M., Turberville, J.M., Linford, L.S., Rivera, M.C., Garey, J.R., Raff, R.A. et al. (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387, 489493.CrossRefGoogle ScholarPubMed
Blaurock, A.E. (1986) X-ray and neutron diffraction by membranes: how great is the potential for determining the molecular interactions? In Watts, A. and DePont, J.J.H.H.M. (eds) Progress in Protein–Lipid Interactions. Elsevier Amsterdam, vol. 2, pp. 143.Google Scholar
Bullock, T.H. (1984) Comparative neuroethology of startle rapid escape and giant-fiber mediated responses. In Eaton, R.C. (ed.) Neural Mechanisms of Startle Behavior. Plenum Press, pp. 113.Google Scholar
Cardone, B. and Roots, B.I. (1990) Characterization of the myelin-like membranes in earthworm CNS using immunolabelling techniques. Society for Neuroscience Abstracts 16, 666.Google Scholar
Cardone, B. and Roots, B.I. (1991) Comparative studies of myelin-like membranes in annelids and arthropods. Transactions of the American Society for Neurochemistry 22, 148.Google Scholar
Cardone, B. and Roots, B.I. (1996) Monoclonal antibodies to proteins of the myelin-like sheath of earthworm giant axons show cross-reactivity to crayfish CNS glia: an immunogold electronmicroscopy study. Neurochemical Research 21, 505510.CrossRefGoogle Scholar
Chandler, W.K. and Meves, H. (1965) Voltage clamp experiments in internally perfused giant axons. Journal of Physiology (London) 180, 788820.CrossRefGoogle ScholarPubMed
Coggeshall, R.E. (1965) A fine structural analysis of the ventral nerve cord and associated sheath of Lumbricus terrestris L. Journal of Comparative Neurology 125, 393437.CrossRefGoogle ScholarPubMed
Davis, A.D., Weatherby, T.M., Hartline, D.K. and Lenz, P.H. (1999) Myelin-like sheaths in copepod axons. Nature 398, 571.CrossRefGoogle ScholarPubMed
Drewes, C.P. and Brinkhurst, R.O. (1990) Glial nerve fibres and rapid escape reflexes in newly hatched aquatic oligochaetes Lumbriculus variegatus (family Lumbriculidae). Invertebrate Reproduction and Development 17, 9195.CrossRefGoogle Scholar
Drummond, G.I., Iyer, N.T. and Keith, J. (1962) Hydrolysis of ribonucleoside 2′3′-cyclic phosphates by a diesterase from brain. Journal of Biological Chemistry 237, 35353539.CrossRefGoogle Scholar
Dunn, C.W., Hejnol, A., Matus, D.Q., Pang, K., Browne, W.E., Smith, S.A. et al. (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452, 745749.CrossRefGoogle ScholarPubMed
Fernández, I., Pardos, F., Benito, J. and Roldán, C. (1996) Ultrastructural observations on the phoronid nervous system. Journal of Morphology 230, 265281.3.0.CO;2-D>CrossRefGoogle ScholarPubMed
Govind, C.K. and Pearce, J. (1988) Remodeling of nerves during claw reversal in adult snapping shrimps. Journal of Comparative Neurology 268, 121130.CrossRefGoogle ScholarPubMed
Graham, A. (2000) Animal phylogeny: Root and branch surgery. Current Biology 10, R36R38.CrossRefGoogle ScholarPubMed
Günther, J. (1973) A new type of ‘node’ in the myelin sheath of an invertebrate nerve fibre. Experientia 29, 12631265.CrossRefGoogle ScholarPubMed
Günther, J. (1976) Impulse conduction in the myelinated giant fibres of the earthworm. Structure and function of the dorsal nodes in the median giant fibre. Journal of Comparative Neurology 168, 505531.CrossRefGoogle Scholar
Hama, K. (1959) Some observations on the fine structure of the giant nerve fibres of the earthworm Eisenia foetida. Journal of Biophysical and Biochemical Cytology 6, 6166.CrossRefGoogle ScholarPubMed
Hama, K. (1966) The fine structure of the Schwann cell sheath of the nerve fiber in the shrimp (Penaeus japonicus). Journal of Cell Biology 31, 624632.CrossRefGoogle ScholarPubMed
Heuser, J.E. and Doggenweiler, C.F. (1966) The fine structural organization of nerve fibers, sheaths, and glial cells in the prawn Palaemonetes vulgaris. Journal of Cell Biology 30, 381403.CrossRefGoogle ScholarPubMed
Holmes, W. (1942) The giant myelinated nerve fibres of the prawn. Philosophical Transactions of the Royal Society London Series B 231, 293311.Google Scholar
Holmes, W., Pumphrey, R.J. and Young, J.Z. (1941) The structure and conduction velocity of the medullated nerve fibres of prawns. Journal of Experimental Biology 18, 5054.CrossRefGoogle Scholar
Hsu, K. and Terakawa, S. (1996) Fenestration in the myelin sheath of nerve fibers of the shrimp: a novel node of excitation for saltatory conduction. Journal of Neurobiology 30, 397409.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
Jenner, R.A. (2004) The scientific status of metazoan cladistics: why current research practice must change. Zoologica Scripta 33, 293310.CrossRefGoogle Scholar
Jones, M. and Gardiner, S. (1989) On the early development of the vestimentiferan tube worm Ridgeia sp. and observations on the nervous system and trophosome of Ridgeia sp. and Riftia pachyptila. Biological Bulletin 177, 254276.CrossRefGoogle Scholar
Kusano, K. (1966) Electrical activity and structural correlates of giant nerve fibers in Kuruma shrimp (Penaeus japonicus). Journal of Cellular Physiology 68, 301383.CrossRefGoogle Scholar
Kusano, K. and LaVail, M.M. (1971) Impulse conduction in the shrimp medullated giant fiber with special reference to the structure of functionally excitable areas. Journal of Comparative Neurology 142, 481494.CrossRefGoogle Scholar
Lenz, P.H., Hartline, D.K. and Davis, A.D. (2000) The need for speed. I. Fast reactions and myelinated axons in copepods. Journal of Comparative Physiology A 186, 337345.CrossRefGoogle Scholar
Levinson, S.R. and Meves, H. (1975) The binding of tritiated tetrodotoxin to squid giant axons. Philosophical Transactions of the Royal Society London Series B 270, 349352.Google ScholarPubMed
Mazumder, R., Iyer, L.M., Vasudevan, S. and Aravind, L. (2002) Detection of novel members, structure-function analysis and evolutionary classification of the 2H phosphoesterase superfamily. Nucleic Acids Research 30, 52295243.CrossRefGoogle ScholarPubMed
McAlear, J.H., Milburn, N.S., Chapman, G.B. (1958) The fine structure of Schwann cells, nodes of Ranvier and Schmidt–Lanterman incisures in the central nervous system of the crab Cancer irroratus. Journal of Ultrastructural Research 2, 171176.CrossRefGoogle ScholarPubMed
Nageotte, J. (1916) Note sur les fibres a myéline et sur les étranglements de Ranvier chez certains crustacés. Comptes rendus des scéances de la Société de biologie et de ses filiales Paris 79, 259263.Google Scholar
Neumcke, B. and Stämpfli, R. (1982) Sodium currents and sodium-current fluctuations in rat myelinated nerve fibres. Journal of Physiology (London) 329, 163184.CrossRefGoogle ScholarPubMed
Nicol, J.A.C. (1948) The giant axons of annelids. Quarterly Review of Biology 23, 291323.Google ScholarPubMed
Nonner, W., Rojas, E. and Stämpfli, R. (1975) Gating currents in the node of Ranvier: voltage and time dependence. Philosophical Transactions of the Royal Society London Series B 270, 483492.Google ScholarPubMed
Okamura, N., Stoskopf, M., Hendricks, F. and Kishimoto, Y. (1985a) Phylogenetic dichotomy of nerve glycerosphingolipids. Proceedings of the National Academy of Sciences of the U.S.A. 82, 67796782.CrossRefGoogle Scholar
Okamura, N., Stoskopf, M., Yamaguchi, H. and Kishimoto, Y. (1985b) Lipid composition of the nervous system of earthworms (Lumbricus terrestris). Journal of Neurochemistry 45, 18751879.CrossRefGoogle ScholarPubMed
Okamura, N., Yamaguchi, H., Stuskopf, M., Kishimoto, Y. and Saida, T. (1986) Isolation and characterization of multilayered sheath membrane rich in glucocerebroside from shrimp ventral nerve. Journal of Neurochemistry 47, 11111116.CrossRefGoogle Scholar
Pereyra, P. and Roots, B.I. (1988) Isolation and initial characterization of myelin-like membrane fractions from the nerve cord of earthworms (Lumbricus terrestris L.). Neurochemical Research 13, 893901.CrossRefGoogle ScholarPubMed
Pereyra, P., Horvath, E. and Braun, P.E. (1988) Triton X-100 extractions of central nervous system myelin indicate a possible role for the minor myelin proteins in the stability of lamellae. Neurochemical Research 13, 583595.CrossRefGoogle ScholarPubMed
Retzius, G. (1890) Zur Kenntniss des Nervensystems der Crustaceen. Biologische Untersuchungen [N.S.] 1, 150.Google Scholar
Ritchie, J.M., Rogart, R.B. and Strichartz, G. (1976) A new method for labelling sagitoxin and its binding to non-myelinated fibres of the rabbit vagus, lobster walking and garfish olfactory nerves. Journal of Physiology (London) 261, 477494.CrossRefGoogle Scholar
Roots, B.I. (1978) A phylogenetic approach to the anatomy of glia. In Schoffeniels, E. Franck, B. Hertz, L. and Towers, D.B. (eds) Dynamic Properties of Glial Cells. Pergamon Press, New York, pp. 4554.Google Scholar
Roots, B.I. (1981) Comparative studies on glial markers. Journal of Experimental Biology 95, 167180.CrossRefGoogle ScholarPubMed
Roots, B.I. (1984) Evolutional aspects of the structure and function of the nodes of Ranvier. In Zagoren, J.C. and Fedoroff, S. (eds) The Node of Ranvier. Academic Press, Orlando, Fl, pp. 129.Google Scholar
Roots, B.I. (1993) The evolution of myelin. In Malhotra, S. (ed.) Advances in Neural Science, vol. 1, JAI Press Inc., Greenwich, CT, pp. 187213.Google Scholar
Roots, B.I. (1995) The evolution of myelinating cells. In Vernadakis, A. and Roots, B. (eds) Neuron-Glia Interrelations During Phylogeny: I. Phylogeny and Ontogeny of Glial Cells. Humana Press Inc., Totawa, New Jersey, pp. 223248.CrossRefGoogle Scholar
Roots, B.I. and Lane, N.J. (1983) Myelinating glia of earthworm giant axons: thermally-induced intramembranous changes. Tissue & Cell 15, 695709.CrossRefGoogle ScholarPubMed
Roots, B.I. and Gould, R.M. (2007) Evolution of myelinated systems. In Bullock, T.H. Rubenstein, J.L.R. and Kaas, J.H. (eds) Evolution of Nervous Systems Vol. 3 – Evolution of Nervous Systems in Non-Mammalian Vertebrates. Elsevier Ltd, pp. 469484.Google Scholar
Rousset, V., Pleijel, F., Rouse, G.W., Erséus, C. and Siddall, M.E. (2007) A molecular phylogeny of annelids. Cladistics 23, 4163.CrossRefGoogle ScholarPubMed
Sakamoto, Y., Tanaka, N., Ichimiya, T., Kurihara, T. and Nakamura, K.T. (2005) Crystal structure of the catalytic fragment of human brain 2′3′-cyclic-nucleotide 3′-phosphodiesterase. Journal of Molecular Biology 346, 789800.CrossRefGoogle Scholar
Schweigreiter, R., Roots, B.I., Bandtlow, C.E. and Gould, R.M. (2006) Understanding myelination through studying its evolution. International Review of Neurobiology 73, 219273.CrossRefGoogle ScholarPubMed
Sigworth, F.J. (1980) The variance of sodium current fluctuations at the node of Ranvier. Journal of Physiology (London) 307, 97129.CrossRefGoogle ScholarPubMed
da Silva, S.F., Bressan, C.M., Cavalcante, L.A. and Allodi, S. (2003) Binding of an antibody against noncompact myelin protein to presumptive glial cells in the visual system of the crab Ucides cordatus. Glia 43, 292298.CrossRefGoogle ScholarPubMed
Tamai, Y., Kojima, A., Saito, S., Takayama-Abe, K. and Horichi, H. (1992) Characteristic distribution of glycolipids in gadoid fish nerve tissues and its bearing on phylogeny. Journal of Lipid Research 33, 13511359.CrossRefGoogle ScholarPubMed
Taylor, D.P., Dyer, K.A. and Newburgh, R.W. (1976) Cyclic nucleotides in neuronal and glial enriched fractions from the nerve cord of Manduca sexta. Journal of Insect Physiology 22, 13031304.CrossRefGoogle ScholarPubMed
Taylor, G.W. (1940) The optical properties of the earthworm giant fiber sheath as related to fiber size. Journal of Cellular and Comparative Physiology 15, 363371.CrossRefGoogle Scholar
Terakawa, S. and Hsu, K. (1991) Ionic currents of the nodal membrane underlying the fastest saltatory conduction in myelinated giant nerve fibers of the shrimp Penaeus japonicus. Journal of Neurobiology 22, 342352.CrossRefGoogle ScholarPubMed
Waehneldt, T.V., Malotka, J., Kitamura, S. and Kishimoto, Y. (1989) Electrophoretic characterization and immunoblot analysis of the proteins from the myelin-like light membrane fraction of shrimp ventral nerve (Penaeus duorarum). Comparative Biochemistry and Physiology 92B, 369374.Google Scholar
Weatherby, T.M., Davis, A.D., Hartline, D.K. and Lenz, P.H. (2000) The need for speed. II. Myelin in calanoid copepods. Journal of Comparative Physiology A 186, 347357.CrossRefGoogle ScholarPubMed
Wilson, C. and Hartline, D.K. (2007) The development of calanoid copepod myelin. Program No. 674.8. 2007 Neuroscience Meeting Planner. San Diego, CA: Society for Neuroscience 2007. Online.Google Scholar
Wilson, C. and Hartline, D.K. (2008) A non-glial source of myelin in copepods? Program No. 79.23. 2008 Neuroscience Meeting Planner. Washington, DC: Society for Neuroscience 2008. Online.Google Scholar
Xu, K. and Terakawa, S. (1999) Fenestration nodes and the wide submyelinic space form the basis for the unusually fast impulse conduction of shrimp myelinated axons. Journal of Experimental Biology 202, 19791989.Google ScholarPubMed
Zoran, M.J., Drewes, C.D., Fourtner, C.R. and Siegel, A.J. (1988) The lateral giant fibers of the Tubificid worm Branchiura sowerbyi: structural and functional asymmetry in a paired interneuronal system. Journal of Comparative Neurology 275, 7686.CrossRefGoogle Scholar