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Evidence for the prepattern/cooption model of vertebrate jaw evolution

Cerny, Robert and Cattell, Maria and Sauka-Spengler, Tatjana and Yu, Feiqiao and Meulemans Medeiros, Daniel and Bronner-Fraser, Marianne (2010) Evidence for the prepattern/cooption model of vertebrate jaw evolution. Proceedings of the National Academy of Sciences of the United States of America, 107 (40). pp. 17262-17267. ISSN 0027-8424. PMCID PMC2951391. https://resolver.caltech.edu/CaltechAUTHORS:20101025-111202869

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Abstract

The appearance of jaws was a turning point in vertebrate evolution because it allowed primitive vertebrates to capture and process large, motile prey. The vertebrate jaw consists of separate dorsal and ventral skeletal elements connected by a joint. How this structure evolved from the unjointed gill bar of a jawless ancestor is an unresolved question in vertebrate evolution. To understand the developmental bases of this evolutionary transition, we examined the expression of 12 genes involved in vertebrate pharyngeal patterning in the modern jawless fish lamprey. We find nested expression of Dlx genes, as well as combinatorial expression of Msx, Hand and Gsc genes along the dorso-ventral (DV) axis of the lamprey pharynx, indicating gnathostome-type pharyngeal patterning evolved before the appearance of the jaw. In addition, we find that Bapx and Gdf5/6/7, key regulators of joint formation in gnathostomes, are not expressed in the lamprey first arch, whereas Barx, which is absent from the intermediate first arch in gnathostomes, marks this domain in lamprey. Taken together, these data support a new scenario for jaw evolution in which incorporation of Bapx and Gdf5/6/7 into a preexisting DV patterning program drove the evolution of the jaw by altering the identity of intermediate first-arch chondrocytes. We present this “Pre-pattern/Cooption” model as an alternative to current models linking the evolution of the jaw to the de novo appearance of sophisticated pharyngeal DV patterning.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1073/pnas.1009304107 DOIArticle
http://www.pnas.org/content/107/40/17262.abstractPublisherArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2951391/PubMed CentralArticle
http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1009304107/-/DCSupplementalPublisherSupporting Information
ORCID:
AuthorORCID
Sauka-Spengler, Tatjana0000-0001-9289-0263
Bronner-Fraser, Marianne0000-0003-4274-1862
Additional Information:© 2010 by the National Academy of Sciences. Edited by Clifford J. Tabin, Harvard Medical School, Boston, MA, and approved August 31, 2010 (received for review July 2, 2010). We thank Roger Bergstedt, Deborah Winkler, Nikolas Rewald, and Kathy Jones (Hammond Bay Biological Station, Millersburg, MI) for generously supplying adult lampreys; Gage Crump and David Stock for critical reading of the manuscript; and two anonymous reviewers whose comments helped improve this work. R.C. was supported by the Grant Agency of the Academy of Sciences of the Czech Republic (206/07/P257) and by Ministry of Education, Youth, and Sports Project 0021620828. M.C. and D.M.M. were supported by National Science Foundation Grant IOS0920751 (to D.M.M.). T.S.-S. was supported by National Institutes of Health Grant DE017911 (to M.B.-F.). Author contributions: D.M.M. designed research; R.C., M.C., F.Y., and D.M.M. performed research; T.S.-S. and M.B.-F. contributed new reagents/analytic tools; R.C. and D.M.M. analyzed data; and D.M.M. wrote the paper. The authors declare no conflict of interest. Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. HQ248098–HQ248103). This article is a PNAS Direct Submission. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1009304107/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
Academy of Sciences of the Czech Republic206/07/P257
Ministry of Education, Youth, and Sports (Czech Republic)0021620828
NSFIOS0920751
NIHDE017911
Subject Keywords:vertebrate; jaw; evolution; pharynx; lamprey
Issue or Number:40
PubMed Central ID:PMC2951391
Record Number:CaltechAUTHORS:20101025-111202869
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20101025-111202869
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:20503
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:29 Nov 2010 19:23
Last Modified:09 Mar 2020 13:19

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