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Open Access Research article

The homology of odontodes in gnathostomes: insights from Dlx gene expression in the dogfish, Scyliorhinus canicula

Mélanie Debiais-Thibaud135, Silvan Oulion136, Franck Bourrat4, Patrick Laurenti12, Didier Casane12 and Véronique Borday-Birraux12*

Author affiliations

1 Evolution des familles multigéniques, Laboratoire Evolution Génome et Spéciation, UPR9034 CNRS, 1 avenue de la terrasse, 91198 Gif-sur-Yvette, France

2 UFR des Sciences du Vivant, Université Paris Diderot Sorbonne Paris Cité, 5 rue Marie-Andrée Lagroua Weill-Hallé, 75205 Paris Cedex 13, France

3 UFR Sciences, Université Paris-Sud 11, 91405 Orsay Cedex, France

4 Laboratoire Neurobiologie et Développement, Institut de Neurobiologie Alfred Fessard, UPR3294 CNRS, 1 avenue de la terrasse, 91198 Gif-sur-Yvette, France

5 Département Forme, Institut des Sciences de l'Evolution - Montpellier, UMR5554 CNRS/Université Montpellier II, Place Eugène Bataillon, 34095 Montpellier cedex05, France

6 Evolution et développement des chordés, Biologie Intégrative des Organismes Marins, UMR7232 CNRS/UMPC Université Paris 6, Observatoire océanologique, Avenue du Fontaulé, 66650 Banyuls-sur-Mer, France

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Citation and License

BMC Evolutionary Biology 2011, 11:307  doi:10.1186/1471-2148-11-307

Published: 18 October 2011

Abstract

Background

Teeth and tooth-like structures, together named odontodes, are repeated organs thought to share a common evolutionary origin. These structures can be found in gnathostomes at different locations along the body: oral teeth in the jaws, teeth and denticles in the oral-pharyngeal cavity, and dermal denticles on elasmobranch skin. We, and other colleagues, had previously shown that teeth in any location were serially homologous because: i) pharyngeal and oral teeth develop through a common developmental module; and ii) the expression patterns of the Dlx genes during odontogenesis were highly divergent between species but almost identical between oral and pharyngeal dentitions within the same species. Here we examine Dlx gene expression in oral teeth and dermal denticles in order to test the hypothesis of serial homology between these odontodes.

Results

We present a detailed comparison of the first developing teeth and dermal denticles (caudal primary scales) of the dogfish (Scyliorhinus canicula) and show that both odontodes develop through identical stages that correspond to the common stages of oral and pharyngeal odontogenesis. We identified six Dlx paralogs in the dogfish and found that three showed strong transcription in teeth and dermal denticles (Dlx3, Dlx4 and Dlx5) whereas a weak expression was detected for Dlx1 in dermal denticles and teeth, and for Dlx2 in dermal denticles. Very few differences in Dlx expression patterns could be detected between tooth and dermal denticle development, except for the absence of Dlx2 expression in teeth.

Conclusions

Taken together, our histological and expression data strongly suggest that teeth and dermal denticles develop from the same developmental module and under the control of the same set of Dlx genes. Teeth and dermal denticles should therefore be considered as serial homologs developing through the initiation of a common gene regulatory network (GRN) at several body locations. This mechanism of heterotopy supports the 'inside and out' model that has been recently proposed for odontode evolution.