Distinct ossification trade-offs illuminate the shoulder girdle reconfiguration at the water-to-land transition

Janet Wei, Thomas W. P. Wood, Kathleen Flaherty, Olivia E. Fitch, Shahid Ali, Alyssa Enny, Ali Andrescavage, Danielle Brazer, Dina Navon, Hannah E. Cohen, Derek Gordon, Anusha Shanabag, Shunya Kuroda, Thomas A. Stewart, Ingo Braasch and Tetsuya Nakamura ()
Additional contact information
Janet Wei: Rutgers the State University of New Jersey
Thomas W. P. Wood: Rutgers the State University of New Jersey
Kathleen Flaherty: Rutgers the State University of New Jersey
Olivia E. Fitch: Michigan State University
Shahid Ali: University of Chicago
Alyssa Enny: Rutgers the State University of New Jersey
Ali Andrescavage: Rutgers the State University of New Jersey
Danielle Brazer: Rutgers the State University of New Jersey
Dina Navon: INSPIRE Program, Robert Wood Johnson Medical School
Hannah E. Cohen: Rutgers the State University of New Jersey
Derek Gordon: Rutgers the State University of New Jersey
Anusha Shanabag: Rutgers the State University of New Jersey
Shunya Kuroda: Rutgers the State University of New Jersey
Thomas A. Stewart: University Park
Ingo Braasch: Michigan State University
Tetsuya Nakamura: Rutgers the State University of New Jersey

Nature Communications, 2025, vol. 16, issue 1, 1-16

Abstract: Abstract The mechanisms of the pectoral girdle transformation at the origin of terrestrial locomotion in vertebrates remain an outstanding problem. The loss of intramembranous bones and the enlargement of endochondral bones resulted in the disarticulation of the pectoral girdle from the skull and the formation of the neck during the fish-to-tetrapod transition. Despite the functional implications of this skeletal shift in the emergence of terrestrial vertebrates, the underlying genetic-developmental alterations have remained enigmatic. Here, we show that in zebrafish pectoral girdle mesodermal cells expressing gli3, a transcription factor gene in the Hedgehog signaling pathway, differentiate into both intramembranous and endochondral bones. Intriguingly, Gli and Hedgehog compound knockout fish exhibited an unexpected combination of actinopterygian fish and stem-tetrapod pectoral girdle characteristics. These ontogenetic and anatomical data suggest that a trade-off between the two distinct ossification pathways is a deeply embedded developmental program in bony fishes and that tuning of this trade-off can generate novel pectoral girdle akin to those of stem-tetrapods at the dawn of vertebrate terrestrialization.

Date: 2025
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DOI: 10.1038/s41467-025-60236-z

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