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The Origin of the Myelination Program in Vertebrates

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The Origin of the Myelination Program in Vertebrates View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Magazine R511 (2005) showed furthermore that the potentials along non-myelinated same chromosomal regions from the Correspondences invertebrate axons propagate at Bogotá X chromosome cause both about 1 m sec−1 or less for an the hybrid male sterility and meiotic axon of ~10 µm in diameter. This drive. Genetic mapping studies have The origin of is sufficient, however, for routine to date been unable to break up the conduction within the framework association between male sterility and the myelination of animals of relatively small size meiotic drive, suggesting that the two program in (between 0.1 and 30 cm) [4]. Among phenomena may be causally linked invertebrates, only the cephalopods (Orr et al., 2007). vertebrates (squid, octopus) have larger axons, These studies show that X but this large size is generally chromosome drive may contribute limited to those neurons involved to reproductive isolation between B. Zalc1,2, D. Goujet3, and D. Colman4 in the rapid ‘escape’ response. By diverging lineages and thus promote increasing the diameter of key axons species diversification. However, The myelin sheath was a up to 1 mm or more, cephalopods as noted above, X drive can hinder transformative vertebrate have increased action potential adaptive evolution within lineages acquisition, enabling great increases speed, and so have been able to if it goes unsuppressed. Although in impulse propagation velocity evolve a larger body size. it has been over 80 years since X along axons. Not all vertebrates It should be noted that, in many drive was first reported, it is only very possess myelinated axons, however, invertebrate species, certain axons recently that the larger evolutionary and when myelin first appeared are covered with what are best implications have become appreciated. in the vertebrate lineage is an characterized as ‘experimental’ As more species are subject to genetic important open question. It has forms of myelin [5–7], and indeed, and genomic research, we will get a been suggested that the dual, these axons conduct at much higher better idea of the pervasiveness of this apparently unrelated acquisitions velocities than their diameters phenomenon and its effects. of myelin and the hinged jaw were would otherwise permit if they were actually coupled in evolution [1,2]. bare. These devices work well for Acknowledgments If so, it would be expected that organisms with multiple ganglia, I’d like to thank Catherine Montchamp- myelin was first acquired during the but must have been unsatisfactory Moreau and Yun Tao for helpful comments Devonian period by the oldest jawed for vertebrates, which, because of on the manuscript. fish, the placoderms [3]. Although the physical constraints imposed myelin itself is not retained in the by the skull and vertebral column, Further reading fossil record, within the skulls of evolved instead a complex program Cazemajor, M., Joly, D., and Montchamp-Moreau, C. (2000). Sex-ratio meiotic drive in Drosophila fossilized Paleozoic vertebrate fish to ensheath axons within a tightly simulans is related to equational nondisjunction are exquisitely preserved imprints compacted insulating membrane: of the Y chromosome. Genetics 154, 229–236. Derome, N., Baudry, E., Ogereau, D., Veuille, M., of cranial nerves and the foramina the vertebrate myelin sheath and Montchamp-Moreau, C. (2008). Selective they traversed. Examination of that enables action potentials to sweeps in a 2-locus model for sex-ratio meiotic these structures now suggests how propagate at 50 to 100 m sec−1 drive in Drosophila simulans. Mol. Biol. Evol. 25, 409–416. the nerves functioned in vivo. In along axons with a diameter similar Dyer, K.A., Charlesworth, B., and Jaenike, J. (2007). placoderms, the first hinge-jawed to most invertebrates (Supplemental Chromosome-wide linkage disequilibrium as a consequence of meiotic drive. Proc. Natl. Acad. fish, oculomotor nerve diameters Results 1 in the Supplemental data Sci. USA 104, 1587–1592. remained constant, but nerve available online). Frank, S.A. (1991). Divergence of meiotic drive- lengths were ten times longer than It occurred to us that fossil fish suppression systems as an explanation for sex-biased hybrid sterility and inviability. in the jawless osteostraci. We infer might harbor some clues as to Evolution 45, 262–267. that to accommodate this ten-fold Hurst, L.D., and Pomiankowski, A. (1991). Causes of sex-ratio bias may account for unisexual sterility increase in length, while maintaining in hybrids: a new explanation of Haldane’s rule a constant diameter, the oculomotor HAGFISH and related phenomena. Genetics 128, 841–858. system in placoderms must have Lyttle T.W. (1991). Segregation distorters. Annu. Rev. Genet. 25, 511–557. been myelinated to function as a LAMPREYS Orr, H.A., and Irving, S. (2005). Segregation rapidly conducting motor pathway. distortion in hybrids between the Bogotá and USA subspecies of Drosophila pseudoobscura. Placoderms were the first fish with OSTEOSTRACI † ES Genetics 169, 671–682. hinged jaws and some can grow AT Orr, H.A., Masly, J.P., and Phadnis, N. (2007). † S to formidable lengths, requiring a PLACODERMS CRANI Speciation in Drosophila: from phenotypes to TE rapid conduction system, so it is molecules. J. Hered. 98, 103–110. EBRA RT Tao, Y., Hartl, D.L., and Laurie, C.C. (2001). Sex- CHONDRICHTHYANS A VE highly likely that they were the first AT ratio segregation distortion associated with OM reproductive isolation in Drosophila. Proc. Natl. organisms with myelinated axons in ACANTHODIANS † HOST Acad. Sci. USA 98, 13183–13188. the craniate lineage. AT Tao, Y., Masly, J.P., Araripe, L., Ke, Y., and Hartl, In non-myelinated axons, the ACTINOPTERYGIANS GN D.L. (2007). A sex-ratio meiotic drive system in Drosophila simulans. I: An autosomal propagation speed of the action SARCOPTERYGIANS suppressor. PloS Biol. 5, 2560–2575. potential is directly proportional ‘BONYFISHES’ Current Biology to the axon diameter. In both Department of Biology, University of vertebrates and invertebrates, axon Rochester, Rochester, New York 14627, USA. diameter averages between 0.5 and Figure 1. Fish cladogram (according to [8,9]). E-mail: [email protected] 30 µm. As a consequence, action indicates extinct taxa. Current Biology Vol 18 No 12 R512 whether their peripheral nerves aspirating sea water along the ocean were myelinated or not. It might bottom to filter for food. be expected that the nerve length: The evidence we have presented diameter ratio would be smaller in here supports the view that myelin non-myelinated than in myelinated appeared initially in the first animal species, as is indeed the case in with a hinged jaw, the placoderm. It living animals. Accordingly, we set out is our opinion that the myelin sheath to determine this ratio for Paleozoic in vertebrates arose in conjunction vertebrate fish — osteostraci and with the neural crest, which gives placoderms (Figure 1) — that were rise to the jaw apparatus and contemporaneous, and for whom most of the peripheral nervous rare well-preserved fossilized skulls system. The myelin sheath was an exist (Supplemental Results 2 in the extraordinary enabling acquisition Supplemental data). in this regard, facilitating both We examined the skulls of predatory and escape behaviors, several fossil osteostraci and and permitting the evolution of very placoderms, measured the lengths large vertebrate body sizes such of the oculomotor (n.III) nerves and as were featured in the placoderm compared them with the diameter repertoire. of the nerves as inferred from the sizes of the oculomotor foramina Supplemental data at their exit points from the skull. Supplemental data are available at http:// We focused our attention on the www.current-biology.com/cgi/content/ oculomotor nerve primarily for full/18/12/R511/DC1 technical reasons: The foramen Acknowledgments of n.III was easily traced in our D.R.C. was supported by a grant from NIH specimens, and importantly, this (NS20147) and B.Z. by Inserm. nerve runs a straight course within the skull, so its length can be easily References and reliably measured. 1. Colman, D.R., Doyle, J.P., Kitagawa, K., It is striking that for foramen D’Urso, D., Pedraza, L., Yoshida, M., and Fannon, A.M. (1995). Speculations on myelin diameters of about the same width sheath evolution. In: Glial Cell Development. (0.1 mm), the length of the nerve K. Jessen and W.D. Richardson, eds. (Oxford: Bios Scientific Publication). in osteostraci was about ten-times 2. Richardson, W.D., Pringle, N.P., Yu, W.P., shorter than that in placoderms, and Hall, A.C. (1997). Origins of spinal cord consistent with the notion that myelin oligodendrocytes: possible developmental and evolutionary relationships with motor was a feature of the placoderm neurons. Dev. Neurosci. 19, 58–68. nervous system, but was absent in 3. Zalc, B., and Colman, D.R. (2000). Origin of vertebrate success. Science 288, 271–272. the osteostraci (Figure 2 and Table S1 4. Grassé, P.P. (1975). Le système nerveux des in the Supplemental data). We insectes. In Traité de Zoologie, PP. Grassé also noted that the great increase (ed.), T.VIII, Vol.III, 321–510. 5. Hartline, D.K., and Colman, D.R. (2007). Rapid in oculomotor nerve length in conduction and the evolution of giant axons placoderms corresponds to a two and myelinated fibers. Curr. Biol. 17, R29–R35. 6. Pereyra, P.M., and Roots, B.I. (1988). Isolation fold increase in the length of the face. and initial characterization of myelin-like If one assumes that in placoderms membrane fractions from the nerve cord myelination of n.III was most likely of earthworms (Lumbricus terrestris L). Neurochem. Res. 13, 893–901. a necessity for rapid tracking 7. Davis, A.D., Weatherby, T.M., Hartline, D.K., movement of the eye to fulfill the and Lenz, P.H.
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