Evolutionary Trends of the Pharyngeal Dentition in Cypriniformes (Actinopterygii: Ostariophysi)

International audienceBACKGROUND: The fish order Cypriniformes is one of the most diverse ray-finned fish groups in the world with more than 3000 recognized species. Cypriniformes are characterized by a striking distribution of their dentition: namely the absence of oral teeth and presence of pharyngeal teeth on the last gill arch (fifth ceratobranchial). Despite this limited localisation, the diversity of tooth patterns in Cypriniformes is astonishing. Here we provide a further description of this diversity using X-ray microtomography and we map the resulting dental characters on a phylogenetic tree to explore evolutionary trends. RESULTS: We performed a pilot survey of dental formulae and individual tooth shapes in 34 adult species of Cypriniformes by X-ray microtomography (using either conventional X-ray machine, or synchrotron microtomography when necessary) or by dissecting. By mapping morphological results in a phylogenetic tree, it emerges that the two super-families Cobitoidea and Cyprinoidea have followed two distinct evolutionary pathways. Furthermore, our analysis supports the hypothesis of a three-row dentition as ancestral for Cyprinoidea and a general trend in tooth row reduction in most derived lineages. Yet, this general scheme must be considered with caution as several events of tooth row gain and loss have occurred during evolutionary history of Cyprinoidea. SIGNIFICANCE: Dentition diversity in Cypriniformes constitutes an excellent model to study the evolution of complex morphological structures. This morphological survey clearly advocates for extending the use of X-ray microtomography to study tooth morphology in Cypriniformes. Yet, our survey also underlines that improved knowledge of Cypriniformes life traits, such as feeding habits, is required as current knowledge is not sufficient to conclude on the link between diet and dental morphology

Evolution of pharyngeal dentition in Cypriniformes

Les Cypriniformes sont un ordre de poissons téléostéens d’eau douce composé d’environ 4000 espèces. Ils sont caractérisés par l’absence de dents orales et la présence de dents pharyngiennes uniquement sur le cinquième cératobranchial. Cependant, par rapport à d’autres groupes, leur denture pharyngienne présente une diversité très importante en termes de nombre et surtout de forme de dents. J’ai donc étudié l’étendue de la diversité de la denture pharyngienne chez les Cypriniformes, dans un cadre phylogénétique, permettant ainsi de mettre en évidence des tendances évolutives. Au sein des Cypriniformes, j’ai étudié certains groupes plus en détail, au regard de leur importance et de leur diversité. J’ai cherché à comprendre quels pouvaient être les facteurs expliquant la diversité de la denture pharyngienne et il s’avère que ces facteurs sont différents selon les groupes de Cypriniformes étudiés. Alors que le régime alimentaire semble être un facteur essentiel chez les Cyprininae, cela n’est pas le cas chez les Leuciscinae pour lesquels il y a surtout un héritage phylogénétique important. Chez un autre groupe, les Danioninae, c’est en revanche le type de développement qui explique la diversité des dents pharyngiennes. Cette étude détaillée de la diversité de la denture pharyngienne des Cypriniformes va permettre d’utiliser ce groupe comme nouveau modèle d’évo-dévo des dents grâce au poisson-zèbre qui est un modèle de biologie du développement. Dans ce cadre, une première étude d’un mutant chez le poisson-zèbre a permis de mettre en évidence le rôle de l’acide rétinoïque dans le développement et l’évolution du nombre et de la forme des dents chez les Cypriniformes. Ce travail a donc permis d’explorer la diversité de la denture pharyngiennes des Cypriniformes, de mettre en évidence des tendances évolutives et de comprendre certains facteurs à l’origine de cette évolution.Cypriniformes are the most diverse freshwater fish clade with around 4,000 species. They are characterized by the absence of oral teeth and the presence of pharyngeal teeth restricted to the fifth ceratobranchials. Yet, compared to other groups, their pharyngeal dentition displays a huge diversity both in terms of number and shape. I have investigated the extant of the diversity of the pharyngeal dentition in Cypriniformes, in a phylogenetic framework, allowing to decipher evolutionary trends. I have studied several groups within Cypriniformes in more details, because of their importance in terms of diversity. I have tried to understand what factors could explain this diversity of pharyngeal dentition and it appeared that those factors could be different according to each group. Whereas diet and other ecological factors are important in Cyprininae, it is not the case in Leuciscinae in which there are essentially phylogenetic signals. In another group, Danioninae, it is the type of development which explains the diversity of pharyngeal dentition. This detailed study of the diversity of pharyngeal dentition in Cypriniformes will allow to use this group as a new model of Evo/devo of teeth thanks to the zebrafish, which is already a model in developmental biology. In this context, a first study of a zebrafish mutant displaying dental defects has shown the role of retinoic acid in the development and the evolution of tooth number and shape in Cypriniformes.This work is an exploration of the diversity of the pharyngeal dentition in Cypriniformes, allowing to point out evolutionary trends and to understand factors that account for the evolution of pharyngeal teeth

Comments on 'The valid generic names for the fish species usually placed in Cyclocheilichthys' (KOTTELAT 2013) and a correction of Pasco-viel et al. (2012)

Pasco-Viel, Emmanuel, Veran, Monette, Viriot, Laurent (2013): Comments on 'The valid generic names for the fish species usually placed in Cyclocheilichthys' (KOTTELAT 2013) and a correction of Pasco-viel et al. (2012). Zootaxa 3640 (3): 483-484, DOI: http://dx.doi.org/10.11646/zootaxa.3640.3.1

Altered retinoic acid signalling underpins dentition evolution

Small variations in signalling pathways have been linked to phenotypic diversity and speciation. In vertebrates, teeth represent a reservoir of adaptive morphological structures that are prone to evolutionary change. Cyprinid fish display an impressive diversity in tooth number, but the signals that generate such diversity are unknown. Here, we show that retinoic acid (RA) availability influences tooth number size in Cyprinids. Heterozygous adult zebrafish heterozygous for the cyp26b1 mutant that encodes an enzyme able to degrade RA possess an extra tooth in the ventral row. Expression analysis of pharyngeal mesenchyme markers such as dlx2a and lhx6 shows lateral, anterior and dorsal expansion of these markers in RA-treated embryos, whereas the expression of the dental epithelium markers dlx2b and dlx3b is unchanged. Our analysis suggests that changes in RA signalling play an important role in the diversification of teeth in Cyprinids. Our work illustrates that through subtle changes in the expression of rate-limiting enzymes, the RA pathway is an active player of tooth evolution in fish

Retinoic acid controls tooth morphology and number in cypriniformes

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Phylogeny and polyploidy: Resolving the classification of cyprinine fishes (Teleostei: Cypriniformes)

Cyprininae is the largest subfamily (>1300 species) of the family Cyprinidae and contains more polyploid species (similar to 400) than any other group of fishes. We examined the phylogenetic relationships of the Cyprininae based on extensive taxon, geographical, and genomic sampling of the taxa, using both mitochondria] and nuclear genes to address the phylogenetic challenges posed by polyploidy. Four datasets were analyzed in this study: two mitochondria] gene datasets (465 and 791 taxa, 5604 bp), a mitogenome dataset (85 taxa, 14,771 bp), and a cloned nuclear RAG1 dataset (97 taxa, 1497 bp). Based on resulting trees, the subfamily Cyprininae was subdivided into 11 tribes: Probarbini (new; Probarbus + Catlocarpio), Labeonini Bleeker, 1859 (Labeo & allies), Torini Karaman, 1971 (Tor, Labeobarbus & allies), Smiliogastrini Bleeker, 1863 (Puntius, Enteromius & allies), Poropuntiini (Poropuntius & allies), Cyprinini Rafinesque, 1815 (Cyprinus & allies), Acrossocheilini (new; Acrossocheilus & allies), Spinibarbini (new; Spinibarbus), Schizothoracini McClelland, 1842 (Schizothorax & allies), Schizopygopsini Mirza, 1991 (Schizopygopsis & allies), and Barbini Bleeker, 1859 (Barbus & allies). Phylogenetic relationships within each tribe were discussed. Two or three distinct RAG1 lineages were identified for each of the following tribes Torini, Cyprinini, Spinibarbini, and Barbini, indicating their hybrid origin. The hexaploid African Labeobarbus & allies and Western Asian Capoeta are likely derived from two independent hybridization events between their respective maternal tetraploid ancestors and Cyprinion. (C) 2015 Elsevier Inc. All rights reserved