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

Nature Ecology & Evolutionvolume 1pages17311736 (2017) | Download Citation

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.

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A correction to this article is available online at https://doi.org/10.1038/s41559-017-0374-5.

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.

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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

Author notes

    • Koh Onimaru

    Present address: Phyloinformatics Unit, RIKEN Center for Life Science Technologies (CLST), 2-2-3, Minatojima-Minamimachi, Chuo-ku, Kobe, Hyogo, 650-0047, Japan

Affiliations

  1. School of Life Science and Technology, Tokyo Institute of Technology, B-17, 4259 Nagatsuta-cho, Midori-ku, Yokohama, 226-8501, Japan

    • Eri Okamoto
    • , Koh Onimaru
    •  & Mikiko Tanaka
  2. Evolutionary Morphology Laboratory, RIKEN, 2-2-3 Minatojima-Minamimachi, Chuo-ku, Kobe, Hyogo, 650-0047, Japan

    • Rie Kusakabe
    •  & Shigeru Kuratani
  3. Phyloinformatics Unit, RIKEN Center for Life Science Technologies (CLST), 2-2-3, Minatojima-Minamimachi, Chuo-ku, Kobe, Hyogo, 650-0047, Japan

    • Shigehiro Kuraku
  4. Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba, 227-8564, Japan

    • Susumu Hyodo
  5. EMBL-CRG Systems Biology Research Unit, Centre for Genomic Regulation (CRG) and Universitat Pompeu Fabra (UPF), Spain Doctor. Aiguader 88, 08003, Barcelona, Spain

    • Alexandre Robert-Moreno
    •  & James Sharpe

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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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Mikiko Tanaka.

Electronic supplementary material

  1. Supplemental Figures

    Supplementary Figures 1-5.

  2. Supplementary Video 1

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

  3. Supplementary Video 2

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

  4. Supplementary Video 3

    OPT-scanned S. canicula embryos at stage 26.

  5. Supplementary Video 4

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

  6. Supplementary Video 5

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

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DOI

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

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