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

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          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.

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          Most cited references37

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          SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny.

          SEAVIEW and PHYLO_WIN are two graphic tools for X Windows-Unix computers dedicated to sequence alignment and molecular phylogenetics. SEAVIEW is a sequence alignment editor allowing manual or automatic alignment through an interface with CLUSTALW program. Alignment of large sequences with extensive length differences is made easier by a dot-plot-based routine. The PHYLO_WIN program allows phylogenetic tree building according to most usual methods (neighbor joining with numerous distance estimates, maximum parsimony, maximum likelihood), and a bootstrap analysis with any of them. Reconstructed trees can be drawn, edited, printed, stored, evaluated according to numerous criteria. Taxonomic species groups and sets of conserved regions can be defined by mouse and stored into sequence files, thus avoiding multiple data files. Both tools are entirely mouse driven. On-line help makes them easy to use. They are freely available by anonymous ftp at biom3.univ-lyon1.fr/pub/ mol_phylogeny or http:@acnuc.univ-lyon1.fr/, or by e-mail to galtier@biomserv.univ-lyon1.fr.
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            The cutting-edge of mammalian development; how the embryo makes teeth.

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              Molecular evidence on the evolutionary and biogeographical patterns of European cyprinids.

              The phylogenetic relationships of 106 European cyprinid taxa were determined based on the complete nucleotide sequence (1140 bp) of the mitochondrial cytochrome b gene. The molecular phylogeny was used (1) to revise the current systematics of European cyprinids, (2) to establish the phylogenetic utility of traditional morphological characters that are widely used in Cyprinidae systematics, and (3) to discuss alternative hypotheses on the biogeography of the family in Europe. The age of the major lineages within European cyprinids was tentatively estimated with a molecular clock and showed full agreement with the fossil record of the group. Moreover, the results provided unambiguous evidence for a close phylogenetic affinity of some Caucasian and Greek endemic cyprinid taxa (e.g., B. capito and B. brachycephalus and Leuciscus keadicus, Barbus graecus, and B. albanicus, respectively) to Iberian and North African, but not Central European, cyprinids. The existence of such unexpected phylogenetic relationships refutes the classical hypothesis on the biogeography of European cyprinids, which assumes a dispersal of the cyprinid fauna from central Europe to southern Europe and northern Africa during the Miocene (and, hence, predicts a close phylogenetic relationship of all Caucasian, Greek, Iberian, and North African cyprinids to central European taxa). Instead, the existence of a Mediterranean realm independent of the central European route seems plausible based on the molecular evidence. It is likely that the new biogeographical scenario proposed here might apply to other primary freshwater European animals with low dispersal abilities, including fish, amphibians, and invertebrates.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2010
                24 June 2010
                : 5
                : 6
                : e11293
                Affiliations
                [1 ]Evo-devo of Vertebrate Dentition, Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, CNRS, INRA, Ecole Normale Supérieure de Lyon, Lyon, France
                [2 ]Molecular Zoology, Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, CNRS, INRA, Ecole Normale Supérieure de Lyon, Lyon, France
                [3 ]iPHEP, CNRS UMR 6046, Université de Poitiers, Poitiers, France
                [4 ]European Synchrotron Radiation Facility, Grenoble, France
                Centre for Genomic Regulation (CRG), Universitat Pompeu Fabra, Spain
                Author notes

                Conceived and designed the experiments: LV VL. Performed the experiments: EPV CC PT LV. Analyzed the data: EPV PC MS. Wrote the paper: EPV LV VL.

                [¤]

                Current address: Department of Orofacial Sciences, University of California San Francisco, San Francisco, California, United States of America

                Article
                09-PONE-RA-13865R2
                10.1371/journal.pone.0011293
                2892034
                20585584
                261aac7c-78c0-4236-b319-9595979ce2b6
                Pasco-Viel et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 28 October 2009
                : 31 May 2010
                Page count
                Pages: 15
                Categories
                Research Article
                Developmental Biology/Developmental Evolution
                Developmental Biology/Pattern Formation
                Evolutionary Biology/Developmental Evolution
                Evolutionary Biology/Paleontology

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                Uncategorized

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