Co-option of neck muscles supported the vertebrate water-to-land transition
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...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-12-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-54724-x |
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| author | Eglantine Heude Hugo Dutel Frida Sanchez-Garrido Karin D. Prummel Robert Lalonde France Lam Christian Mosimann Anthony Herrel Shahragim Tajbakhsh |
| author_facet | Eglantine Heude Hugo Dutel Frida Sanchez-Garrido Karin D. Prummel Robert Lalonde France Lam Christian Mosimann Anthony Herrel Shahragim Tajbakhsh |
| author_sort | Eglantine Heude |
| collection | DOAJ |
| description | 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. |
| format | Article |
| id | doaj-art-45186d618c3a413bb63203b852629c7e |
| institution | OA Journals |
| issn | 2041-1723 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-45186d618c3a413bb63203b852629c7e2025-08-20T02:30:59ZengNature PortfolioNature Communications2041-17232024-12-011511910.1038/s41467-024-54724-xCo-option of neck muscles supported the vertebrate water-to-land transitionEglantine Heude0Hugo Dutel1Frida Sanchez-Garrido2Karin D. Prummel3Robert Lalonde4France Lam5Christian Mosimann6Anthony Herrel7Shahragim Tajbakhsh8Institut de Génomique Fonctionnelle de Lyon, École Normale Supérieure de Lyon, CNRS UMR5242 Université Claude Bernard Lyon-1Bristol Palaeobiology Research Group, School of Earth Sciences, University of BristolPHYMA, Département Adaptations du Vivant, Muséum national d’Histoire naturelle, CNRS UMR 7221Department of Molecular Life Sciences, University of ZurichDepartment of Pediatrics, Section of Developmental Biology, University of Colorado School of Medicine, Anschutz Medical CampusCore Facilities - Institut de Biologie Paris Seine (IBPS), Sorbonne UniversitésDepartment of Molecular Life Sciences, University of ZurichMECADEV, Département Adaptations du Vivant, Muséum national d’Histoire naturelle, CNRS UMR 7179Department of Developmental & Stem Cell Biology, Stem Cells & Development Unit, Institut Pasteur, Université Paris CitéAbstract 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.https://doi.org/10.1038/s41467-024-54724-x |
| spellingShingle | Eglantine Heude Hugo Dutel Frida Sanchez-Garrido Karin D. Prummel Robert Lalonde France Lam Christian Mosimann Anthony Herrel Shahragim Tajbakhsh Co-option of neck muscles supported the vertebrate water-to-land transition Nature Communications |
| title | Co-option of neck muscles supported the vertebrate water-to-land transition |
| title_full | Co-option of neck muscles supported the vertebrate water-to-land transition |
| title_fullStr | Co-option of neck muscles supported the vertebrate water-to-land transition |
| title_full_unstemmed | Co-option of neck muscles supported the vertebrate water-to-land transition |
| title_short | Co-option of neck muscles supported the vertebrate water-to-land transition |
| title_sort | co option of neck muscles supported the vertebrate water to land transition |
| url | https://doi.org/10.1038/s41467-024-54724-x |
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