Evolutionary trends of the pharyngeal dentition in Cypriniformes (Actinopterygii: Ostariophysi)

Abstract

Background: 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.

Figure 1. Localization of the fifth ceratobranchial in the goldfish, Carassius auratus (Cyprinidae) and dental plate for this species.

1, 2 and 3 are general views of the whole goldfish skeleton with the fifth ceratobranchial, bearing the pharyngeal teeth, painting in red. 1: Lateral view; 2: Ventral view; 3: Posterior view. 4 is the dental plate for this species with three conventional views: A: Occlusal view; B: ventral view; C: dorsal view. The dental formula for the goldfish is 4/4 (there is, on each side, one row of four teeth). Moreover, on one side, replacement teeth are visible as they are not attached to the pharyngeal bone (pointed by red arrows). The tooth shape is “compressed”.

Figure 2. Examples of Cypriniformes dentitions obtained by microtomography and analysis of 3D reconstructions.

In each case, the dental formula and the tooth shape are indicated. 1: Danio rerio (Rasborinae); 2,4,5; spoon. 2: Carassius auratus (Cyprininae); 4; compressed. 3: Cyprinus carpio (Cyprininae); 1,1,3; molariform. 4: Epalzeorhynchos bicolor (Cyprininae); 2,4,5; spatula. 5: Gobio gobio (Gobioninae); 2,5(−5,3); spoon. 6: Scardinius erythrophtalmus (Leuciscinae); 3,5; saw. 7: Xenocypris yunnanensis (Cultrinae); 2,3,5(−6,3,2); compressed. 8: Misgurnus anguillicaudatus (Cobitidae); 14–16; conical. 9: Ictiobus cyprinellus (Catostomidae); 55; conical. A: occlusal view; B: ventral view; C: dorsal view. Except for 8 and 9. A: anterior view; B: posterior view. For Cyprinoidea plates, teeth are painted according to the following: (i) teeth on the left side are all painted according to their row: red for ventral row, blue for mediodorsal row and yellow for dorsal row; (ii) teeth on the right side are painted only if their row displays a tooth number different from the left side (so that species displaying asymmetry are easily visible because of colours on the right half-bone).

Figure 3. Various morphotypes of Cypriniformes teeth illustrated with examples from our dataset.

A: spoon tooth shape of Puntius semifasciolatus (Cyprininae) with an incurved depressed region and a hook at the end of each tooth; B: spatula tooth shape of Epalzeorhynchos bicolor (Cyprininae), an intermediary form between the spoon and compressed morphologies, with teeth forming a grinding surface; C: compressed tooth shape of Carassius carassius (Cyprininae), with an elongated depressed region; D: conical tooth shape of Catostomus commersonii (Catostomidae); E: saw tooth shape of Scardinius erythrophtalmus (Leuciscinae); F: molariform tooth shape of Cyprinus carpio (Cyprininae).

Figure 4. Pharyngeal dentition of minute Rasborinae.

A: Sundadanio axelrodi, a minute Rasborinae with three tooth rows. B: Rasbora borapetensis and Boraras brigittae, two minute Rasborinae, with two tooth rows.

Figure 5. Phylogenetic relationships within Cypriniformes.

The 50% majority-rule consensus tree obtained by phylogenetic Bayesian analyses, with model GTR+I+Γ, after 5,000,000 generations. Analyses were carried out with four markers whose sequences were downloaded from Genbank: cytb, rag1, rag2 and rho. Posterior probabilities are all indicated on branches. Constraints have been set so that all species are assigned to their respective monophyletic clades determined in previous studies (see Materials and Methods).

Figure 6. Evolution of the character “number of tooth rows” by performing ML analyses on our phylogenetic tree using BayesTraits.

The variants of this character are coded with different colours: each circle in front of species' names is coloured according to the number of tooth rows either determined in our study or found in literature. The ancestral characters inferred by the ML method at different nodes of the tree are given by coloured pies. The proportion of each colour in pies represents the proportion of likelihood for each character state. For tooth row number, the state “0” was not taken into account for the ML analysis (see Materials and Methods).

Figure 7. Evolution of the character “tooth shape” by performing ML analyses on our phylogenetic tree using BayesTraits.

The variants of this character are coded with different colours: each circle in front of species' names is coloured according to the tooth shape determined in our study or found in literature. The ancestral characters inferred by this method at different nodes of the tree are given by coloured pies. The proportion of each colour in pies represents the proportion of likelihood for each character state. For tooth shape, the states “spatula”, “molariform” and “saw” morphotypes were not taken into account for the ML analysis (see Materials&Methods).