Title:
An Ancient Gene Network Is Co-opted for Teeth on Old and New Jaws
An Ancient Gene Network Is Co-opted for Teeth on Old and New Jaws
Author(s)
Fraser, Gareth J.
Hulsey, C. Darrin
Bloomquist, Ryan F.
Uyesugi, Kristine
Manley, Nancy R.
Streelman, J. Todd
Hulsey, C. Darrin
Bloomquist, Ryan F.
Uyesugi, Kristine
Manley, Nancy R.
Streelman, J. Todd
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Abstract
Vertebrate dentitions originated in the posterior pharynx of jawless fishes more than half a billion years ago. As
gnathostomes (jawed vertebrates) evolved, teeth developed on oral jaws and helped to establish the dominance of
this lineage on land and in the sea. The advent of oral jaws was facilitated, in part, by absence of hox gene expression
in the first, most anterior, pharyngeal arch. Much later in evolutionary time, teleost fishes evolved a novel toothed jaw
in the pharynx, the location of the first vertebrate teeth. To examine the evolutionary modularity of dentitions, we
asked whether oral and pharyngeal teeth develop using common or independent gene regulatory pathways. First, we
showed that tooth number is correlated on oral and pharyngeal jaws across species of cichlid fishes from Lake Malawi
(East Africa), suggestive of common regulatory mechanisms for tooth initiation. Surprisingly, we found that cichlid
pharyngeal dentitions develop in a region of dense hox gene expression. Thus, regulation of tooth number is
conserved, despite distinct developmental environments of oral and pharyngeal jaws; pharyngeal jaws occupy hoxpositive,
endodermal sites, and oral jaws develop in hox-negative regions with ectodermal cell contributions. Next, we
studied the expression of a dental gene network for tooth initiation, most genes of which are similarly deployed across
the two disparate jaw sites. This collection of genes includes members of the ectodysplasin pathway, eda and edar,
expressed identically during the patterning of oral and pharyngeal teeth. Taken together, these data suggest that
pharyngeal teeth of jawless vertebrates utilized an ancient gene network before the origin of oral jaws, oral teeth, and
ectodermal appendages. The first vertebrate dentition likely appeared in a hox-positive, endodermal environment and
expressed a genetic program including ectodysplasin pathway genes. This ancient regulatory circuit was co-opted and
modified for teeth in oral jaws of the first jawed vertebrate, and subsequently deployed as jaws enveloped teeth on
novel pharyngeal jaws. Our data highlight an amazing modularity of jaws and teeth as they coevolved during the
history of vertebrates. We exploit this diversity to infer a core dental gene network, common to the first tooth and all
of its descendants.
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Date Issued
2009-02-10
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