TY - JOUR
T1 - Morphogenetic mechanism of the acquisition of the dinosaur-type acetabulum
AU - Egawa, Shiro
AU - Saito, Daisuke
AU - Abe, Gembu
AU - Tamura, Koji
N1 - Funding Information:
Ethics. All animal experiments were properly performed in accordance with guidelines provided by Tohoku University. Data accessibility. The datasets supporting this article have been uploaded as part of the electronic supplementary material. Authors’ contributions. S.E. conceived the project, collected most of the data and prepared the draft of the manuscript. D.S. established molecule-expressing cell lines and cloned some genes for ISH. S.E., D.S., G.A. and K.T. interpreted the results and revised the manuscript. Competing interests. We have no competing interests. Funding. This research was supported by the following grants: JSPS KAKENHI (grant no. JP15J06859) and a Grant for Program Research from the Division for International Advanced Research and Education (DIARE), Tohoku University, to S.E.; JSPS KAKENHI (grant no. 25711015) to D.S. and JSPS KAKENHI (grant no. JP15H04374) to K.T. Acknowledgements. We would like to express our appreciation to T. Hirasawa and S. Kuratani (Riken CDB) for providing turtle embryos for the pilot analysis; K. Bellido, J. Pisenti and K. Portillo (UC Davis Avian Science Facility) for providing the limbless chicken mutant collection; H. Kiyonari (Riken CDB) for providing the gecko-chordin ISH probe; Y. Takahashi (Kyoto University) for providing pT2A-BI-TRE-Gap43-TdTomato; M. Parrish (SJSU) and G.S. Paul for kind permission to reprint the figures of skeletal reconstruction; T. Makino, G. Kumano (Tohoku University) and two reviewers for brushing up the manuscript; M. Hanson (Yale University) for English language editing.
Publisher Copyright:
© 2018 The Authors.
PY - 2018/10/1
Y1 - 2018/10/1
N2 - Understanding morphological evolution in dinosaurs from a mechanistic viewpoint requires the elucidation of the morphogenesis that gave rise to derived dinosaurian traits, such as the perforated acetabulum. In the current study, we used embryos of extant animals with ancestral- and dinosaur-type acetabula, namely, geckos and turtles (with unperforated acetabulum), and birds (with perforated acetabulum). We performed comparative and experimental analyses, focusing on inter-tissue interaction during embryogenesis, and found that the avian perforated acetabulum develops via a secondary loss of cartilaginous tissue in the acetabular region. This cartilage loss might be mediated by inter-tissue interaction with the hip interzone, a mesenchymal tissue that exists in the embryonic joint structure. Furthermore, the data indicate that avian pelvic anlagen is more susceptible to paracrine molecules, e.g. Wnt ligand, secreted by the hip interzone than 'reptilian' anlagen. We hypothesize that during the emergence of dinosaurs, the pelvic anlagen became susceptible to the Wnt ligand, which led to the loss of the cartilaginous tissue and to the perforation in the acetabular region. Thus, the current evolutionary-developmental biology study deepens our understanding of morphological evolution in dinosaurs and provides it with a novel perspective.
AB - Understanding morphological evolution in dinosaurs from a mechanistic viewpoint requires the elucidation of the morphogenesis that gave rise to derived dinosaurian traits, such as the perforated acetabulum. In the current study, we used embryos of extant animals with ancestral- and dinosaur-type acetabula, namely, geckos and turtles (with unperforated acetabulum), and birds (with perforated acetabulum). We performed comparative and experimental analyses, focusing on inter-tissue interaction during embryogenesis, and found that the avian perforated acetabulum develops via a secondary loss of cartilaginous tissue in the acetabular region. This cartilage loss might be mediated by inter-tissue interaction with the hip interzone, a mesenchymal tissue that exists in the embryonic joint structure. Furthermore, the data indicate that avian pelvic anlagen is more susceptible to paracrine molecules, e.g. Wnt ligand, secreted by the hip interzone than 'reptilian' anlagen. We hypothesize that during the emergence of dinosaurs, the pelvic anlagen became susceptible to the Wnt ligand, which led to the loss of the cartilaginous tissue and to the perforation in the acetabular region. Thus, the current evolutionary-developmental biology study deepens our understanding of morphological evolution in dinosaurs and provides it with a novel perspective.
KW - Acetabulum
KW - Dinosaur
KW - Joint development
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U2 - 10.1098/rsos.180604
DO - 10.1098/rsos.180604
M3 - Article
AN - SCOPUS:85056749822
SN - 2054-5703
VL - 5
JO - Royal Society Open Science
JF - Royal Society Open Science
IS - 10
M1 - 180604
ER -