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Co-option of neck muscles supported the vertebrate water-to-land transition

Author

Listed:
  • Eglantine Heude

    (CNRS UMR5242 Université Claude Bernard Lyon-1
    CNRS UMR 7221)

  • Hugo Dutel

    (University of Bristol
    UMR 5199
    Hôpital Necker - Enfants Malades)

  • Frida Sanchez-Garrido

    (CNRS UMR 7221)

  • Karin D. Prummel

    (University of Zurich
    Anschutz Medical Campus
    European Molecular Biology Laboratory (EMBL))

  • Robert Lalonde

    (Anschutz Medical Campus
    Yale University)

  • France Lam

    (Sorbonne Universités)

  • Christian Mosimann

    (University of Zurich
    Anschutz Medical Campus)

  • Anthony Herrel

    (CNRS UMR 7179
    Ghent University
    University of Antwerp
    Naturhistorisches Museum Bern)

  • Shahragim Tajbakhsh

    (Université Paris Cité
    Institut Pasteur)

Abstract

A major event in vertebrate evolution was the separation of the skull from the pectoral girdle and the acquisition of a functional neck, transitions that required profound developmental rearrangements of the musculoskeletal system. The neck is a hallmark of the tetrapod body plan and allows for complex head movements on land. While head and trunk muscles arise from distinct embryonic mesoderm populations, the origins of neck muscles remain elusive. Here, we combine comparative embryology and anatomy to reconstruct the mesodermal contribution to neck evolution. We demonstrate that head/trunk-connecting muscle groups have conserved mesodermal origins in fishes and tetrapods and that the neck evolved from muscle groups present in fishes. We propose that expansions of mesodermal populations into head and trunk domains during embryonic development underpinned the emergence and adaptation of the tetrapod neck. Our results provide evidence for the exaptation of archetypal muscle groups in ancestral fishes, which were co-opted to acquire novel functions adapted to a terrestrial lifestyle.

Suggested Citation

  • Eglantine Heude & Hugo Dutel & Frida Sanchez-Garrido & Karin D. Prummel & Robert Lalonde & France Lam & Christian Mosimann & Anthony Herrel & Shahragim Tajbakhsh, 2024. "Co-option of neck muscles supported the vertebrate water-to-land transition," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54724-x
    DOI: 10.1038/s41467-024-54724-x
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    References listed on IDEAS

    as
    1. Rui Diogo & Robert G. Kelly & Lionel Christiaen & Michael Levine & Janine M. Ziermann & Julia L. Molnar & Drew M. Noden & Eldad Tzahor, 2015. "A new heart for a new head in vertebrate cardiopharyngeal evolution," Nature, Nature, vol. 520(7548), pages 466-473, April.
    2. Frédéric Relaix & Didier Rocancourt & Ahmed Mansouri & Margaret Buckingham, 2005. "A Pax3/Pax7-dependent population of skeletal muscle progenitor cells," Nature, Nature, vol. 435(7044), pages 948-953, June.
    3. Toshiyuki Matsuoka & Per E. Ahlberg & Nicoletta Kessaris & Palma Iannarelli & Ulla Dennehy & William D. Richardson & Andrew P. McMahon & Georgy Koentges, 2005. "Neural crest origins of the neck and shoulder," Nature, Nature, vol. 436(7049), pages 347-355, July.
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