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Evolutionary origins of vertebrate appendicular muscle

Nature volume 408, pages 82–86 (2000)Cite this article

Abstract

The evolution of terrestrial tetrapod species heralded a transition in locomotor strategies. While most fish species use the undulating contractions of the axial musculature to generate propulsive force, tetrapods also rely on the appendicular muscles of the limbs to generate movement1,2. Despite the fossil record generating an understanding of the way in which the appendicular skeleton has evolved to provide the scaffold for tetrapod limb musculature3, there is, by contrast, almost no information as to how this musculature arose. Here we examine fin muscle formation within two extant classes of fish. We find that in the teleost, zebrafish, fin muscles arise from migratory mesenchymal precursor cells that possess molecular and morphogenetic identity with the limb muscle precursors of tetrapod species. Chondrichthyan dogfish embryos, however, use the primitive mechanism of direct epithelial somitic extensions to derive the muscles of the fin. We conclude that the genetic mechanism controlling formation of tetrapod limb muscles evolved before the Sarcopterygian radiation.

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Figure 1: Zebrafish fin muscle formation.
Figure 2: Identification of fin muscle precursors within zebrafish somites.
Figure 3: Expression of zebrafish lbx1 and mox genes.
Figure 4: Fin muscle formation in S. canicula.

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References

  1. Goodrich, E. S. Studies on the Structure and Development of Vertebrates Vol. 1 (Dover Publications, New York/Constable and Company LTD, London, 1958).

    Google Scholar 

  2. Kardong, K. V. Vertebrates, Comparative Anatomy, Function, Evolution (Wm C. Brown, Oxford, 1995).

    Google Scholar 

  3. Coates, M. I. The origin of vertebrate limbs. Development (suppl.) The Evolution of Developmental Mechanisms 169–180 (1994).

  4. Weinberg, E. S. et al. Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos. Development 122, 271–280 (1996).

    CAS  PubMed  Google Scholar 

  5. Devoto, S. H., Melancon, E., Eisen, J. S. & Westerfield, M. Identification of separate slow and fast muscle precursor cells in vivo , prior to somite formation. Development 122, 3371–3380 (1996).

    CAS  PubMed  Google Scholar 

  6. Blagden, C. S., Currie, P. D., Ingham, P. W. & Hughes, S. M. Notochord induction of zebra fish slow muscle is mediated by Sonic Hedgehog. Genes Dev. 11, 2163–2175 (1997).

    Article  CAS  Google Scholar 

  7. Braus, H. Beitrage zur entwicklung der musculatur unddes peripheren nervensystems der selachier. Morphologisches Jahrbuch 27, 501–629 (1899).

    Google Scholar 

  8. Dohrn, A. Die paarigen und unpaaren Flossen der Selachier. Mitteilungen Zoologischen Station Neapol 5, 161–195 (1884).

    Google Scholar 

  9. Corning, H. K. Uber die ventralen urwirbelknopsen in der brustflosse der teleostier. Morphologisches Jahrbuch 22, 79–98 (1842).

    Google Scholar 

  10. Harrison, R. G. Die entwicklung der unpaaren und paarigen flossen der teleostier. Arch. Mikrosk. Anat. EntwMech. 46, 500– 578 (1895).

    Article  Google Scholar 

  11. Grimm, M. Origin of the muscle blastemas in the developing pectoral fin of the rainbow trout (Salmo gairdneri). Folia Morphologica 21, 197–199 (1973).

    Google Scholar 

  12. Higashijima, S., Okamoto, H., Ueno, N., Hotta, Y. & Eguchi, G. High-frequency generation of transgenic zebrafish which reliably express GFP in whole muscles or the whole body by using promoters of zebrafish origin. Dev. Biol. 192, 289 –299 (1997).

    Article  CAS  Google Scholar 

  13. Kozlowski, D. J., Murakami, T., Ho, R. K. & Weinberg, E. S. Regional cell movement and tissue patterning in the zebrafish embryo revealed by fate mapping with caged fluorescein. Biochem. Cell Biol. 75, 551–562 (1997).

    Article  CAS  Google Scholar 

  14. Christ, B., Jacob, H. J. & Jacob, M. Experimental analysis of the origin of the wing musculature in avian embryos. Anat. Embryol. 150, 171 –186 (1977).

    Article  CAS  Google Scholar 

  15. Jagla, K. et al. Mouse Lbx1 and human LBX1 define a novel mammalian homeobox gene family related to the Drosophila lady bird genes. Mech. Dev. 53, 345–356 ( 1995).

    Article  CAS  Google Scholar 

  16. Mankoo, B. S. et al. Mox2 is a component of the genetic hierarchy controlling limb muscle development. Nature 400, 69– 73 (1999).

    Article  ADS  CAS  Google Scholar 

  17. Schafer, K. & Braun, T. Early specification of limb muscle precursor cells by the homeobox gene Lbx1h. Nature Genet. 23, 213–216 (1999).

    Article  CAS  Google Scholar 

  18. Brohmann, H., Jagla, K. & Birchmeier, C. The role of Lbx1 in migration of muscle precursor cells. Development 127, 437– 445 (2000).

    CAS  PubMed  Google Scholar 

  19. Gross, M. K. et al. Lbx1 is required for muscle precursor migration along a lateral pathway into the limb. Development 127, 413–424 (2000).

    CAS  PubMed  Google Scholar 

  20. Rasmussen, A. S. & Arnason, U. J. Phylogenetic studies of complete mitochondrial DNA molecules place cartilaginous fishes within the tree of bony fishes. Mol. Evol. 48, 118–123 (1999).

    Article  ADS  CAS  Google Scholar 

  21. Janvier, P. Major events in vertebrate evolution. Trends Ecol. Evol. 14, 298–299 (1999).

    Article  Google Scholar 

  22. Basden, A. M., Young, G. C., Coates, M. I. & Ritchie, A. The most primitive osteichthyan braincase? Nature 403 , 185–188 (2000).

    Article  ADS  CAS  Google Scholar 

  23. Didier, D. A. Phylogenetic systematics of extant chimeroid fishes (Holocephali, Chimaeroidei). Am. Mus. Novitates 3119, 1– 86 (1995).

    Google Scholar 

  24. Christ, B., Jacob, M & Jacob, H. J. On the origin and development of the ventro-lateral trunk musculature in the avian embryo. An experimental and ultrastructural study. Anat. Embryol. (Berl.) 166, 87– 101 (1983).

    Article  CAS  Google Scholar 

  25. Christ, B. & Ordahl, C. P. Early stages of chick somite development. Anat. Embryol. (Berl.) 191, 381– 396 (1995).

    Article  CAS  Google Scholar 

  26. Cinnamon, Y., Kahane, N. & Kalcheim, C. Characterisation of the early development of specific hypaxial muscles from the ventrolateral myotome. Development 126, 4305–4315 (1999).

    CAS  PubMed  Google Scholar 

  27. Denetclaw W. F. & Ordahl, C. P. The growth of the dermomyotome and formation of early myotome lineages in thoracolumbar somites of chicken embryos. Development 127, 893– 905 (2000).

    PubMed  Google Scholar 

  28. Dietrich, S., Schubert, F. R., Healy C., Sharpe, P. T. & Lumsden, A. Specification of the hypaxial musculature. Development 125, 2235–2249 (1998).

    CAS  PubMed  Google Scholar 

  29. Houzelstein, D. et al. The homeobox gene Msx1 is expressed in a subset of somites, and in muscle progenitor cells migrating into the forelimb. Development 126, 2689–2701 (1999).

    CAS  PubMed  Google Scholar 

  30. Currie, P. D. & Ingham, P. W. Induction of a specific muscle cell type by a hedgehog-like protein in zebrafish. Nature 382, 452–455 (1996).

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

We are indebted to B. Mankoo for his gift of the zebrafish mox clone and for sharing results before publication. We also thank S. Hughes and M. Goulding for antibodies; and M. Buckingham, R. Sporle, N. Rosenthal, N. Hastie, R. Currie and members of the Currie lab for discussion and critical reading of the manuscript. We thank the staff at the University of Glasgow's Milport Marine Station, Isle of Cumbrae, for the supply of S. canicula embryos; T. Chapman and J. Mattocks for animal husbandry; and P. Perry for help with microscopy. K.J. was supported by grants from the Human Frontier Science Program and from the Association Francaise contre les Myopathies (AFM). C.T. and B.T. were supported by funds from the Institut National de la Santé et de la Recherche Médicale, the Centre National de la Recherche Scientifique, the Hopital Universitaire de Strasbourg, the Association de Recherche sur le Cancer and the Ligue Nationale Contre le Cancer. P.D.C. is supported by a MRC career development fellowship and the BBSRC.

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Author notes

  1. C. Neyt, C. Thisse, B. Thisse and P. D. Currie: These authors contributed equally to this work

Authors and Affiliations

  1. Comparative and Developmental Genetics Section, Medical Research Council, Human Genetics Unit, Western General Hospital , Crewe Road, Edinburgh, EH4 2XU, UK

    C. Neyt, L. Haines & P. D. Currie

  2. INSERM U.384, 28, Place Henri Dunant, Clermont Ferrand Cedex,, 63001, France

    K. Jagla

  3. Institut de Génétique Moléculaire et Cellulaire, CNRS/INSERM/ULP, BP 163, ILLKIRCH Cedex, 67404, France

    C. Thisse & B. Thisse

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  1. C. Neyt
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Correspondence to P. D. Currie.

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Neyt, C., Jagla, K., Thisse, C. et al. Evolutionary origins of vertebrate appendicular muscle. Nature 408, 82–86 (2000). https://doi.org/10.1038/35040549

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