Evidence for the prepattern/cooption model of vertebrate jaw evolution
Robert Cerny a, Maria Cattell b, Tatjana Sauka-Spengler c, Marianne Bronner-Fraser c, Feiqiao Yu c, and Daniel Meulemans Medeiros b,1
+Author Affiliations
aDepartment of Zoology, Charles University in Prague, 128 44 Prague, Czech Republic;
bDepartment of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309; and
cDivision of Biology, California Institute of Technology, Pasadena, CA 91125
Edited by Clifford J. Tabin, Harvard Medical School, Boston, MA, and approved August 31, 2010 (received for review July 2, 2010)
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 thatBapx 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.
vertebrate jaw evolution pharynx lamprey
Footnotes
1To whom correspondence should be addressed. E-mail:Daniel.Medeiros@Colorado.edu.
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.
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