Co-option of neck muscles supported the vertebrate water-to-land transition
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.
Authors
- Shahragim Tajbakhsh
- Christian Mosimann (ORCID: https://orcid.org/0000-0002-0749-2576)
- Églantine Heude (ORCID: https://orcid.org/0000-0003-0563-9607)
- Karin D. Prummel (ORCID: https://orcid.org/0000-0001-6077-6407)
- Robert L. Lalonde (ORCID: https://orcid.org/0000-0002-1803-0983)
- Anthony Herrel (ORCID: https://orcid.org/0000-0003-0991-4434)
- Hugo Dutel (ORCID: https://orcid.org/0000-0002-1908-5150)
- Frida Sánchez-Garrido
- France Lam
Institutions
- Université Claude Bernard Lyon 1 (FR)
- École Normale Supérieure de Lyon (FR)
- Hôpital Necker-Enfants Malades (FR)
- Centre National de la Recherche Scientifique (FR)
- University of Antwerp (BE)
- Université de Bordeaux (FR)
- Institut Pasteur (FR)
- University of Zurich (CH)
- Université Paris Cité (FR)
- Ghent University (BE)
- Yale University (US)
- University of Bristol (GB)
- Sorbonne Université (FR)
- Natural History Museum of Bern (CH)
- Institut de Biologie Paris-Seine (FR)
- Muséum national d'Histoire naturelle (FR)
- Institut de Génomique Fonctionnelle de Lyon (FR)
- European Molecular Biology Laboratory (DE)
- Mécanismes Adaptatifs et Evolution (FR)
- European Molecular Biology Laboratory (DE)
- University of Colorado Anschutz Medical Campus (US)
Publication Details
- Journal
- Nature Communications
- Published
- 2024-12-04
- DOI
- https://doi.org/10.1038/s41467-024-54724-x
- Citations
- 1
- Primary Topic
- Congenital heart defects research
- Type
- article
- Field-Weighted Citation Impact
- 0.23
Funders
- National Science Foundation
- Children's Hospital Colorado
- University of Bristol
- Agence Nationale de la Recherche
- European Synchrotron Radiation Facility
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Muséum National d'Histoire Naturelle
- UZH Foundation
- National Institutes of Health
- Foundation for Research in Science and the Humanities
- Natural Environment Research Council
- National Heart, Lung, and Blood Institute
- University of Colorado School of Medicine, Anschutz Medical Campus