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Synchrotron imaging of dentition provides insights into the biology of Hesperornis and Ichthyornis, the “last” toothed birds

BACKGROUND: The dentitions of extinct organisms can provide pivotal information regarding their phylogenetic position, as well as paleobiology, diet, development, and growth. Extant birds are edentulous (toothless), but their closest relatives among stem birds, the Cretaceous Hesperornithiformes and...

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Autores principales: Dumont, Maïtena, Tafforeau, Paul, Bertin, Thomas, Bhullar, Bhart-Anjan, Field, Daniel, Schulp, Anne, Strilisky, Brandon, Thivichon-Prince, Béatrice, Viriot, Laurent, Louchart, Antoine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5034473/
https://www.ncbi.nlm.nih.gov/pubmed/27659919
http://dx.doi.org/10.1186/s12862-016-0753-6
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author Dumont, Maïtena
Tafforeau, Paul
Bertin, Thomas
Bhullar, Bhart-Anjan
Field, Daniel
Schulp, Anne
Strilisky, Brandon
Thivichon-Prince, Béatrice
Viriot, Laurent
Louchart, Antoine
author_facet Dumont, Maïtena
Tafforeau, Paul
Bertin, Thomas
Bhullar, Bhart-Anjan
Field, Daniel
Schulp, Anne
Strilisky, Brandon
Thivichon-Prince, Béatrice
Viriot, Laurent
Louchart, Antoine
author_sort Dumont, Maïtena
collection PubMed
description BACKGROUND: The dentitions of extinct organisms can provide pivotal information regarding their phylogenetic position, as well as paleobiology, diet, development, and growth. Extant birds are edentulous (toothless), but their closest relatives among stem birds, the Cretaceous Hesperornithiformes and Ichthyornithiformes, retained teeth. Despite their significant phylogenetic position immediately outside the avian crown group, the dentitions of these taxa have never been studied in detail. To obtain new insight into the biology of these ‘last’ toothed birds, we use cutting-edge visualisation techniques to describe their dentitions at unprecedented levels of detail, in particular propagation phase contrast x-ray synchrotron microtomography at high-resolution. RESULTS: Among other characteristics of tooth shape, growth, attachment, implantation, replacement, and dental tissue microstructures, revealed by these analyses, we find that tooth morphology and ornamentation differ greatly between the Hesperornithiformes and Ichthyornithiformes. We also highlight the first Old World, and youngest record of the major Mesozoic clade Ichthyornithiformes. Both taxa exhibit extremely thin and simple enamel. The extension rate of Hesperornis tooth dentine appears relatively high compared to non-avian dinosaurs. Root attachment is found for the first time to be fully thecodont via gomphosis in both taxa, but in Hesperornis secondary evolution led to teeth implantation in a groove, at least locally without a periodontal ligament. Dental replacement is shown to be lingual via a resorption pit in the root, in both taxa. CONCLUSIONS: Our results allow comparison with other archosaurs and also mammals, with implications regarding dental character evolution across amniotes. Some dental features of the ‘last’ toothed birds can be interpreted as functional adaptations related to diet and mode of predation, while others appear to be products of their peculiar phylogenetic heritage. The autapomorphic Hesperornis groove might have favoured firmer root attachment. These observations highlight complexity in the evolutionary history of tooth reduction in the avian lineage and also clarify alleged avian dental characteristics in the frame of a long-standing debate on bird origins. Finally, new hypotheses emerge that will possibly be tested by further analyses of avian teeth, for instance regarding dental replacement rates, or simplification and thinning of enamel throughout the course of early avian evolution. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0753-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-50344732016-09-29 Synchrotron imaging of dentition provides insights into the biology of Hesperornis and Ichthyornis, the “last” toothed birds Dumont, Maïtena Tafforeau, Paul Bertin, Thomas Bhullar, Bhart-Anjan Field, Daniel Schulp, Anne Strilisky, Brandon Thivichon-Prince, Béatrice Viriot, Laurent Louchart, Antoine BMC Evol Biol Research Article BACKGROUND: The dentitions of extinct organisms can provide pivotal information regarding their phylogenetic position, as well as paleobiology, diet, development, and growth. Extant birds are edentulous (toothless), but their closest relatives among stem birds, the Cretaceous Hesperornithiformes and Ichthyornithiformes, retained teeth. Despite their significant phylogenetic position immediately outside the avian crown group, the dentitions of these taxa have never been studied in detail. To obtain new insight into the biology of these ‘last’ toothed birds, we use cutting-edge visualisation techniques to describe their dentitions at unprecedented levels of detail, in particular propagation phase contrast x-ray synchrotron microtomography at high-resolution. RESULTS: Among other characteristics of tooth shape, growth, attachment, implantation, replacement, and dental tissue microstructures, revealed by these analyses, we find that tooth morphology and ornamentation differ greatly between the Hesperornithiformes and Ichthyornithiformes. We also highlight the first Old World, and youngest record of the major Mesozoic clade Ichthyornithiformes. Both taxa exhibit extremely thin and simple enamel. The extension rate of Hesperornis tooth dentine appears relatively high compared to non-avian dinosaurs. Root attachment is found for the first time to be fully thecodont via gomphosis in both taxa, but in Hesperornis secondary evolution led to teeth implantation in a groove, at least locally without a periodontal ligament. Dental replacement is shown to be lingual via a resorption pit in the root, in both taxa. CONCLUSIONS: Our results allow comparison with other archosaurs and also mammals, with implications regarding dental character evolution across amniotes. Some dental features of the ‘last’ toothed birds can be interpreted as functional adaptations related to diet and mode of predation, while others appear to be products of their peculiar phylogenetic heritage. The autapomorphic Hesperornis groove might have favoured firmer root attachment. These observations highlight complexity in the evolutionary history of tooth reduction in the avian lineage and also clarify alleged avian dental characteristics in the frame of a long-standing debate on bird origins. Finally, new hypotheses emerge that will possibly be tested by further analyses of avian teeth, for instance regarding dental replacement rates, or simplification and thinning of enamel throughout the course of early avian evolution. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0753-6) contains supplementary material, which is available to authorized users. BioMed Central 2016-09-23 /pmc/articles/PMC5034473/ /pubmed/27659919 http://dx.doi.org/10.1186/s12862-016-0753-6 Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Dumont, Maïtena
Tafforeau, Paul
Bertin, Thomas
Bhullar, Bhart-Anjan
Field, Daniel
Schulp, Anne
Strilisky, Brandon
Thivichon-Prince, Béatrice
Viriot, Laurent
Louchart, Antoine
Synchrotron imaging of dentition provides insights into the biology of Hesperornis and Ichthyornis, the “last” toothed birds
title Synchrotron imaging of dentition provides insights into the biology of Hesperornis and Ichthyornis, the “last” toothed birds
title_full Synchrotron imaging of dentition provides insights into the biology of Hesperornis and Ichthyornis, the “last” toothed birds
title_fullStr Synchrotron imaging of dentition provides insights into the biology of Hesperornis and Ichthyornis, the “last” toothed birds
title_full_unstemmed Synchrotron imaging of dentition provides insights into the biology of Hesperornis and Ichthyornis, the “last” toothed birds
title_short Synchrotron imaging of dentition provides insights into the biology of Hesperornis and Ichthyornis, the “last” toothed birds
title_sort synchrotron imaging of dentition provides insights into the biology of hesperornis and ichthyornis, the “last” toothed birds
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5034473/
https://www.ncbi.nlm.nih.gov/pubmed/27659919
http://dx.doi.org/10.1186/s12862-016-0753-6
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