Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Migratory appendicular muscles precursor cells in the common ancestor to all vertebrates

A Publisher Correction to this article was published on 17 October 2017

This article has been updated

Abstract

In amniote embryos, skeletal muscles in the trunk are derived from epithelial dermomyotomes, the ventral margin of which extends ventrally to form body wall muscles. At limb levels, ventral dermomyotomes also generate limb-muscle precursors, an Lbx1-positive cell population that originates from the dermomyotome and migrates distally into the limb bud. In elasmobranchs, however, muscles in the paired fins were believed to be formed by direct somitic extension, a developmental pattern used by the amniote body wall muscles. Here we re-examined the development of pectoral fin muscles in catsharks, Scyliorhinus, and found that chondrichthyan fin muscles are indeed formed from Lbx-positive muscle precursors. Furthermore, these precursors originate from the ventral edge of the dermomyotome, the rest of which extends towards the ventral midline to form body wall muscles. Therefore, the Lbx1-positive, de-epithelialized appendicular muscle precursors appear to have been established in the body plan before the divergence of Chondrichthyes and Osteichthyes.

This is a preview of subscription content

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Fig. 1: Expression of genes involved in muscle development in embryos of the catshark S. canicula.
Fig. 2: Muscle precursors are de-epithelialized from the dermomyotome at the pectoral fin level in catshark S. canicula and S. torazame.
Fig. 3: Muscle precursors derived from the ventral dermomyotome migrate towards the head region and fin buds.

Change history

  • 17 October 2017

    In Fig. 2 of this Article originally published, some erroneous lines appeared on the left side of the images in panels c, e and g. The figure should have appeared as shown below. These errors have now been corrected in all versions of the Article.

References

  1. 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).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  3. 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 

  4. 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 

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

    CAS  PubMed  Google Scholar 

  6. Neyt, C. et al. Evolutionary origins of vertebrate appendicular muscle. Nature 408, 82–86 (2000).

    CAS  Article  Google Scholar 

  7. Ochi, H. & Westerfield, M. Lbx2 regulates formation of myofibrils. BMC Dev. Biol. 9, 13 (2009).

    Article  Google Scholar 

  8. Goodrich, E. Studies on the Structure and Development of Vertebrates (Macmillan, London, 1930).

    Book  Google Scholar 

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

    Google Scholar 

  10. Dohrn, A. Die paarigen und unpaaren Flossen der Selachier. Mittheilungen aus der Zoologischen Station zu Neapel 5, 161–195 (1884).

    Google Scholar 

  11. Ballard, W. W., Mellinger, J. & Lechenault, H. A series of normal stages for development of Scyliornius canicula, the lesser spotted dogfish (Chondrichthyes: Scyliohnidae). J. Exp. Zool. 267, 318–336 (1993).

    Article  Google Scholar 

  12. Mennerich, D., Schafer, K. & Braun, T. Pax-3 is necessary but not sufficient for lbx1 expression in myogenic precursor cells of the limb. Mech. Dev. 73, 147–158 (1998).

    CAS  Article  Google Scholar 

  13. Kusakabe, R., Kuraku, S. & Kuratani, S. Expression and interaction of muscle-related genes in the lamprey imply the evolutionary scenario for vertebrate skeletal muscle, in association with the acquisition of the neck and fins. Dev. Biol. 350, 217–227 (2011).

    CAS  Article  Google Scholar 

  14. Kusakabe, R. & Kuratani, S. Evolution and developmental patterning of the vertebrate skeletal muscles: perspectives from the lamprey. Dev. Dynam. 234, 824–834 (2005).

    Article  Google Scholar 

  15. Minchin, J. E. et al. Oesophageal and sternohyal muscle fibres are novel Pax3-dependent migratory somite derivatives essential for ingestion. Development 140, 2972–2984 (2013).

    CAS  Article  Google Scholar 

  16. Chen, F., Liu, K. C. & Epstein, J. A. Lbx2, a novel murine homeobox gene related to the Drosophila ladybird genes is expressed in the developing urogenital system, eye and brain. Mech. Dev. 84, 181–184 (1999).

    CAS  Article  Google Scholar 

  17. Lou, Q., He, J., Hu, L. & Yin, Z. Role of lbx2 in the noncanonical Wnt signaling pathway for convergence and extension movements and hypaxial myogenesis in zebrafish. Biochim. Biophys. Acta 1823, 1024–1032 (2012).

    CAS  Article  Google Scholar 

  18. Jacob, M., Christ, B. & Jacob, H. J. The migration of myogenic cells from the somites into the leg region of avian embryos. An ultrastructural study. Anat. Embryol. 157, 291–309 (1979).

    CAS  Article  Google Scholar 

  19. Brand-Saberi, B., Muller, T. S., Wilting, J., Christ, B. & Birchmeier, C. Scatter factor/hepatocyte growth factor (SF/HGF) induces emigration of myogenic cells at interlimb level in vivo. Dev. Biol. 179, 303–308 (1996).

    CAS  Article  Google Scholar 

  20. Bladt, F., Riethmacher, D., Isenmann, S., Aguzzi, A. & Birchmeier, C. Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376, 768–771 (1995).

    CAS  Article  Google Scholar 

  21. Dietrich, S. et al. The role of SF/HGF and c-Met in the development of skeletal muscle. Development 126, 1621–1629 (1999).

    CAS  PubMed  Google Scholar 

  22. Mackenzie, S., Walsh, F. S. & Graham, A. Migration of hypoglossal myoblast precursors. Dev. Dynam. 213, 349–358 (1998).

    CAS  Article  Google Scholar 

  23. Lours-Calet, C. et al. Evolutionarily conserved morphogenetic movements at the vertebrate head–trunk interface coordinate the transport and assembly of hypopharyngeal structures. Dev. Biol. 390, 231–246 (2014).

    CAS  Article  Google Scholar 

  24. Takagi, W. et al. Hepatic and extrahepatic distribution of ornithine urea cycle enzymes in holocephalan elephant fish (Callorhinchus milii). Comp. Biochem. Physiol. B 161, 331–340 (2012).

    CAS  Article  Google Scholar 

  25. Didier, D. A., Leclair, E. E. & Vanbuskirk, D. R. Embryonic staging and external features of development of the chimaeroid fish, Callorhinchus milii (Holocephali, Callorhinchidae). J. Morphol. 236, 25–47 (1998).

    Article  Google Scholar 

  26. Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994).

    CAS  Article  Google Scholar 

  27. Tamura, K. et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739 (2011).

    CAS  Article  Google Scholar 

  28. Sharpe, J. et al. Optical projection tomography as a tool for 3D microscopy and gene expression studies. Science 296, 541–545 (2002).

    CAS  Article  Google Scholar 

  29. Kawamoto, T. Use of a new adhesive film for the preparation of multi-purpose fresh-frozen sections from hard tissues, whole-animals, insects and plants. Arch. Histol. Cytol. 66, 123–143 (2003).

    Article  Google Scholar 

  30. Oisi, H., Ota, K. G., Kuraku, S. & Kuratani, S. Craniofacial development of hagfishes and the evolution of vertebrates. Nature 10, 175–180 (2013).

    Article  Google Scholar 

  31. Kaneko, H., Nakatani, Y., Fujimura, K. & Tanaka, M. Development of the lateral plate mesoderm in medaka Oryzias latipes and Nile tilapia Oreochromis niloticus: |insight into the diversification of pelvic fin position. J. Anat. 225, 659–674 (2014).

    Article  Google Scholar 

  32. Nakaya, Y., Sukowati, E. W., Wu, Y. & Sheng, G. RhoA and microtubule dynamics control cell-basement membrane interaction in EMT during gastrulation. Nat. Cell Biol. 10, 765–774 (2008).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank A. Tweedale and staff of the Station Biologique de Roscoff for collecting S. canicula embryos, J. D. Bell for collecting C. milii embryos, Y. Yamamoto and K. Ikeda for electron microscopy studies and Y. Oisi and S. Higuchi for technical support. This work was supported in part by a Grant-in-Aid for Scientific Research (B) (25291086) (16H04828) and the Inamori Foundation to M.T., a Grant-in-Aid for Scientific Research (C) (16K07384) to R.K., the Japan–Australia Research Cooperative Program to S.H., the Spanish Ministry of Economy and Competitiveness, ‘Centro de Excelencia Severo Ochoa 2013–2017’, SEV-2012-0208 to J.S., and a Grant-in-Aid for Scientific Research (A) (15H02416) to S.Kurat.

Author information

Authors and Affiliations

Authors

Contributions

M.T., E.O., R.K. and S.Kurat. designed the project and wrote the manuscript, J.S. supervised OPT analyses, and E.O. performed most experiments, except the following experiments. S.Kurak. assisted with sequence identification and molecular phylogenetic analyses, S.H. collected C. milii embryos and provided related materials, A.R.-M. performed OPT analyses, and K.O. assisted with cloning and phylogenetic analyses.

Corresponding author

Correspondence to Mikiko Tanaka.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Supplemental Figures

Supplementary Figures 1-5.

Supplementary Video 1

3D-reconstructed S. canicula embryos at stage 27.

Supplementary Video 2

3D-reconstructed S. canicula embryos at stage 28.

Supplementary Video 3

OPT-scanned S. canicula embryos at stage 26.

Supplementary Video 4

OPT-scanned S. canicula embryos at early stage 27.

Supplementary Video 5

OPT-scanned S. canicula embryos at early stage 28.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Okamoto, E., Kusakabe, R., Kuraku, S. et al. Migratory appendicular muscles precursor cells in the common ancestor to all vertebrates. Nat Ecol Evol 1, 1731–1736 (2017). https://doi.org/10.1038/s41559-017-0330-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-017-0330-4

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing