Abstract
Adaptive evolution has shaped vertebrate skeletal morphology, supporting diverse locomotor modes and lifestyles. In volant birds (carinates), the sternum develops a ventral keel for the attachment of massive pectoral muscles essential for powered flight. In contrast, flightless ratites lack both flight and the keel, creating a marked contrast in sternal shape. Here, we interrogated the cellular and molecular basis underlying this divergence using chicken and emu embryos as models. Through a series of analyses including spatiotemporal transcriptomics and a spheroid culture system, we found that TGF-β signaling, which promotes proliferation of sternal chondroprogenitors, is activated in both species until the left and right progenitors meet. In chicken, this activation persists, driving ventral extension of the keel primordium, whereas in emu it shuts off early, preventing keel formation. Our findings suggest that skeletal morphological changes associated with behavioral transitions can emerge from heterochronic shifts in developmental signaling, thereby deepening our understanding of the evolutionary logic shaping skeletal diversification.
Similar content being viewed by others
Acknowledgements
We greatly acknowledge Dr. Clifford J. Tabin (Harvard Medical School) for careful reading of the manuscript, as well as Drs. Daisuke Saito, Yoshiki Hayashi, Yoshinao Hosaka (Kyushu University), Kengo Buma and Yoshiko Takahashi (Kyoto University) for helpful discussion. We also thank the Center for Advanced Instrumental and Educational Support of the Faculty of Agriculture (Kyushu University) and Transcriptomics Kenkyukai (General incorporated association, Fukuoka) for the use of Cryostar NX70 (Thermo-Fisher Scientific) and RNA-Seq support, respectively. This work was supported by Research Support Project for Life Science and Drug Discovery (Basis for Supporting Innovative Drug Discovery and Life Science Research [BINDs]) from AMED under Grant Number JP23ama121017 and JP25ama121017 (to Y.A.). This study was also funded by the JST FOREST Program (Grant Number JPMJFR214G to Y.A.), JST SPRING (Grant Number JPMJSP2136 to S.J.K.), JSPS KAKENHI (Grant Numbers JP25K09649 to Y.A. and JP24KJ1793 to S.J.K.), The Sumitomo Foundation (to Y.A.), and The Takeda Science Foundation (to Y.A.).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Source data
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Kwon, S.J., Zou, Z., Honda, M. et al. Heterochronic activation of TGF-β signaling drives the diversity of the avian sterna. Nat Commun (2026). https://doi.org/10.1038/s41467-026-72602-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/s41467-026-72602-6
