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Published July 25, 2023 | Published + Supplemental Material
Journal Article Open

Ancient vertebrate dermal armor evolved from trunk neural crest


Bone is an evolutionary novelty of vertebrates, likely to have first emerged as part of ancestral dermal armor that consisted of osteogenic and odontogenic components. Whether these early vertebrate structures arose from mesoderm or neural crest cells has been a matter of considerable debate. To examine the developmental origin of the bony part of the dermal armor, we have performed in vivo lineage tracing in the sterlet sturgeon, a representative of nonteleost ray-finned fish that has retained an extensive postcranial dermal skeleton. The results definitively show that sterlet trunk neural crest cells give rise to osteoblasts of the scutes. Transcriptional profiling further reveals neural crest gene signature in sterlet scutes as well as bichir scales. Finally, histological and microCT analyses of ray-finned fish dermal armor show that their scales and scutes are formed by bone, dentin, and hypermineralized covering tissues, in various combinations, that resemble those of the first armored vertebrates. Taken together, our results support a primitive skeletogenic role for the neural crest along the entire body axis, that was later progressively restricted to the cranial region during vertebrate evolution. Thus, the neural crest was a crucial evolutionary innovation driving the origin and diversification of dermal armor along the entire body axis.

Additional Information

© 2023 the Author(s). Published by PNAS. This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND). The project has received funding from the European Union's Horizon 2020 research and innovation program under Marie Sklodowska-Curie grant agreement No. 897949 (to J.S.) and from National Institutes of Health grant R35NS111564 to (M.E.B). D.C. and P.E.A. were supported by a Wallenberg Scholarship from the Knut & Alice Wallenberg Foundation, awarded to P.E.A. M.L.M. was supported by a fellowship from the Helen Hay Whitney Foundation and by NIH grant 1K99HD100587. J.S., R.F., and M.P. were supported by the Ministry of Education, Youth and Sports of the Czech Republic—project Biodiversity (CZ.02.1.01/0.0/0.0/16_025/0007370) and the Czech Science Foundation (No. 20-23836S). R.C. was supported by the Czech Science Foundation (No. 19-18634S). Gar work in the Braasch Lab is supported by NSF EDGE FGT grant #2029216. Author Contributions. J.S., P.E.A., and M.E.B. designed research; J.S., M.L.M., D.C., D.A.R., and R.F. performed research; J.S., D.C., A.P., M.P., I.B., T.H., and R.C. contributed new reagents/analytic tools; J.S., M.L.M., D.C., D.A.R., R.F., and B.D.M. analyzed data; and J.S., D.C., P.E.A., and M.E.B. wrote the paper. Data, Materials, and Software Availability. The RNA-seq data reported in this paper have been deposited in the National Center for Biotechnology Information Gene Expression Omnibus database (accession no. GSE235280) (64). The authors declare no competing interest.

Attached Files

Published - pnas.2221120120.pdf

Supplemental Material - pnas.2221120120.sapp.pdf

Supplemental Material - pnas.2221120120.sd01.csv

Supplemental Material - pnas.2221120120.sd02.csv

Supplemental Material - pnas.2221120120.sm01.avi

Supplemental Material - pnas.2221120120.sm02.avi

Supplemental Material - pnas.2221120120.sm03.avi


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August 22, 2023
January 18, 2024