Synchrotron imaging and Markov Chain Monte Carlo reveal tooth mineralization patterns
Identifieur interne : 002850 ( Pmc/Curation ); précédent : 002849; suivant : 002851Synchrotron imaging and Markov Chain Monte Carlo reveal tooth mineralization patterns
Auteurs : Daniel R. Green [États-Unis] ; Gregory M. Green [États-Unis] ; Albert S. Colman [États-Unis] ; Felicitas B. Bidlack [États-Unis] ; Paul Tafforeau [France] ; Tanya M. Smith [États-Unis, Australie]Source :
- PLoS ONE [ 1932-6203 ] ; 2017.
Abstract
The progressive character of tooth formation records aspects of mammalian life history, diet, seasonal behavior and climate. Tooth mineralization occurs in two stages: secretion and maturation, which overlap to some degree. Despite decades of study, the spatial and temporal pattern of elemental incorporation during enamel mineralization remains poorly characterized. Here we use synchrotron X-ray microtomography and Markov Chain Monte Carlo sampling to estimate mineralization patterns from an ontogenetic series of sheep molars (n = 45 M1s, 18 M2s). We adopt a Bayesian approach that posits a general pattern of maturation estimated from individual- and population-level mineral density variation over time. This approach converts static images of mineral density into a dynamic model of mineralization, and demonstrates that enamel secretion and maturation waves advance at nonlinear rates with distinct geometries. While enamel secretion is ordered, maturation geometry varies within a population and appears to be driven by diffusive processes. Our model yields concrete expectations for the integration of physiological and environmental signals, which is of particular significance for paleoseasonality research. This study also provides an avenue for characterizing mineralization patterns in other taxa. Our synchrotron imaging data and model are available for application to multiple disciplines, including health, material science, and paleontological research.
Url:
DOI: 10.1371/journal.pone.0186391
PubMed: 29049333
PubMed Central: 5648163
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Green</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Department of Human Evolutionary Biology, Harvard University, Cambridge, Massachusetts, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Human Evolutionary Biology, Harvard University, Cambridge, Massachusetts</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Forsyth Institute, Cambridge, Massachusetts, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Forsyth Institute, Cambridge, Massachusetts</wicri:regionArea></affiliation></author><author><name sortKey="Green, Gregory M" sort="Green, Gregory M" uniqKey="Green G" first="Gregory M." last="Green">Gregory M. 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Smith</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Department of Human Evolutionary Biology, Harvard University, Cambridge, Massachusetts, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Human Evolutionary Biology, Harvard University, Cambridge, Massachusetts</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff007"><addr-line>Australian Research Center for Human Evolution, Griffith University, Brisbane, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Australian Research Center for Human Evolution, Griffith University, Brisbane</wicri:regionArea></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The progressive character of tooth formation records aspects of mammalian life history, diet, seasonal behavior and climate. Tooth mineralization occurs in two stages: secretion and maturation, which overlap to some degree. Despite decades of study, the spatial and temporal pattern of elemental incorporation during enamel mineralization remains poorly characterized. Here we use synchrotron X-ray microtomography and Markov Chain Monte Carlo sampling to estimate mineralization patterns from an ontogenetic series of sheep molars (n = 45 M1s, 18 M2s). We adopt a Bayesian approach that posits a general pattern of maturation estimated from individual- and population-level mineral density variation over time. This approach converts static images of mineral density into a dynamic model of mineralization, and demonstrates that enamel secretion and maturation waves advance at nonlinear rates with distinct geometries. While enamel secretion is ordered, maturation geometry varies within a population and appears to be driven by diffusive processes. Our model yields concrete expectations for the integration of physiological and environmental signals, which is of particular significance for paleoseasonality research. This study also provides an avenue for characterizing mineralization patterns in other taxa. Our synchrotron imaging data and model are available for application to multiple disciplines, including health, material science, and paleontological research.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Leeuwenhoeck, A" uniqKey="Leeuwenhoeck A">A Leeuwenhoeck</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hillson, S" uniqKey="Hillson S">S Hillson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Smith, Tm" uniqKey="Smith T">TM Smith</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ungar, Ps" uniqKey="Ungar P">PS Ungar</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Passey, B" uniqKey="Passey B">B Passey</name></author><author><name sortKey="Cerling, T" uniqKey="Cerling T">T Cerling</name></author><author><name sortKey="Schuster, G" uniqKey="Schuster G">G 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">29049333</article-id><article-id pub-id-type="pmc">5648163</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0186391</article-id><article-id pub-id-type="publisher-id">PONE-D-17-13008</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Digestive System</subject><subj-group><subject>Teeth</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Digestive System</subject><subj-group><subject>Teeth</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Head</subject><subj-group><subject>Jaw</subject><subj-group><subject>Teeth</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Head</subject><subj-group><subject>Jaw</subject><subj-group><subject>Teeth</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Physiological Processes</subject><subj-group><subject>Secretion</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Physiological Processes</subject><subj-group><subject>Secretion</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Digestive System</subject><subj-group><subject>Teeth</subject><subj-group><subject>Molars</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Digestive System</subject><subj-group><subject>Teeth</subject><subj-group><subject>Molars</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Head</subject><subj-group><subject>Jaw</subject><subj-group><subject>Teeth</subject><subj-group><subject>Molars</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Head</subject><subj-group><subject>Jaw</subject><subj-group><subject>Teeth</subject><subj-group><subject>Molars</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Eukaryota</subject><subj-group><subject>Animals</subject><subj-group><subject>Vertebrates</subject><subj-group><subject>Amniotes</subject><subj-group><subject>Mammals</subject><subj-group><subject>Ruminants</subject><subj-group><subject>Sheep</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Engineering and Technology</subject><subj-group><subject>Equipment</subject><subj-group><subject>Particle Accelerators</subject><subj-group><subject>Synchrotrons</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Cell Biology</subject><subj-group><subject>Cellular Types</subject><subj-group><subject>Animal Cells</subject><subj-group><subject>Epithelial Cells</subject><subj-group><subject>Ameloblasts</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Biological Tissue</subject><subj-group><subject>Epithelium</subject><subj-group><subject>Epithelial Cells</subject><subj-group><subject>Ameloblasts</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Biological Tissue</subject><subj-group><subject>Epithelium</subject><subj-group><subject>Epithelial Cells</subject><subj-group><subject>Ameloblasts</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Digestive System</subject><subj-group><subject>Teeth</subject><subj-group><subject>Dentin</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Digestive System</subject><subj-group><subject>Teeth</subject><subj-group><subject>Dentin</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Head</subject><subj-group><subject>Jaw</subject><subj-group><subject>Teeth</subject><subj-group><subject>Dentin</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Head</subject><subj-group><subject>Jaw</subject><subj-group><subject>Teeth</subject><subj-group><subject>Dentin</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Physiological Processes</subject><subj-group><subject>Biomineralization</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Physiological Processes</subject><subj-group><subject>Biomineralization</subject></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Synchrotron imaging and Markov Chain Monte Carlo reveal tooth mineralization patterns</article-title><alt-title alt-title-type="running-head">Mammalian tooth mineralization revealed</alt-title></title-group><contrib-group><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-9817-541X</contrib-id><name><surname>Green</surname><given-names>Daniel R.</given-names></name><role content-type="http://credit.casrai.org/">Conceptualization</role><role content-type="http://credit.casrai.org/">Data curation</role><role content-type="http://credit.casrai.org/">Formal analysis</role><role content-type="http://credit.casrai.org/">Funding acquisition</role><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Resources</role><role content-type="http://credit.casrai.org/">Software</role><role content-type="http://credit.casrai.org/">Validation</role><role content-type="http://credit.casrai.org/">Visualization</role><role content-type="http://credit.casrai.org/">Writing – original draft</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib><contrib contrib-type="author"><name><surname>Green</surname><given-names>Gregory M.</given-names></name><role content-type="http://credit.casrai.org/">Formal analysis</role><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Software</role><role content-type="http://credit.casrai.org/">Validation</role><xref ref-type="aff" rid="aff003"><sup>3</sup></xref><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Colman</surname><given-names>Albert S.</given-names></name><role content-type="http://credit.casrai.org/">Formal analysis</role><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Supervision</role><role content-type="http://credit.casrai.org/">Validation</role><xref ref-type="aff" rid="aff005"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bidlack</surname><given-names>Felicitas B.</given-names></name><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff002"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Tafforeau</surname><given-names>Paul</given-names></name><role content-type="http://credit.casrai.org/">Formal analysis</role><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Resources</role><role content-type="http://credit.casrai.org/">Software</role><role content-type="http://credit.casrai.org/">Validation</role><xref ref-type="aff" rid="aff006"><sup>6</sup></xref></contrib><contrib contrib-type="author"><name><surname>Smith</surname><given-names>Tanya M.</given-names></name><role content-type="http://credit.casrai.org/">Funding acquisition</role><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Project administration</role><role content-type="http://credit.casrai.org/">Resources</role><role content-type="http://credit.casrai.org/">Supervision</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff007"><sup>7</sup></xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>Department of Human Evolutionary Biology, Harvard University, Cambridge, Massachusetts, United States of America</addr-line></aff><aff id="aff002"><label>2</label><addr-line>Forsyth Institute, Cambridge, Massachusetts, United States of America</addr-line></aff><aff id="aff003"><label>3</label><addr-line>Physics Department, Stanford University, Palo Alto, California, United States of America</addr-line></aff><aff id="aff004"><label>4</label><addr-line>Kavli Institute for Particle Physics and Cosmology, Stanford University, Palo Alto, California, United States of America</addr-line></aff><aff id="aff005"><label>5</label><addr-line>Department of the Geophysical Sciences, University of Chicago, Chicago, Illinois, United States of America</addr-line></aff><aff id="aff006"><label>6</label><addr-line>European Synchrotron Radiation Facility, Grenoble, France</addr-line></aff><aff id="aff007"><label>7</label><addr-line>Australian Research Center for Human Evolution, Griffith University, Brisbane, Australia</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Halcrow</surname><given-names>Siân E</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>University of Otago, NEW ZEALAND</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><corresp id="cor001">* E-mail: <email>drgreen@fas.harvard.edu</email></corresp></author-notes><pub-date pub-type="epub"><day>19</day><month>10</month><year>2017</year></pub-date><pub-date pub-type="collection"><year>2017</year></pub-date><volume>12</volume><issue>10</issue><elocation-id>e0186391</elocation-id><history><date date-type="received"><day>3</day><month>4</month><year>2017</year></date><date date-type="accepted"><day>29</day><month>9</month><year>2017</year></date></history><permissions><copyright-statement>© 2017 Green et al</copyright-statement><copyright-year>2017</copyright-year><copyright-holder>Green et al</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="pone.0186391.pdf"></self-uri><abstract><p>The progressive character of tooth formation records aspects of mammalian life history, diet, seasonal behavior and climate. Tooth mineralization occurs in two stages: secretion and maturation, which overlap to some degree. Despite decades of study, the spatial and temporal pattern of elemental incorporation during enamel mineralization remains poorly characterized. Here we use synchrotron X-ray microtomography and Markov Chain Monte Carlo sampling to estimate mineralization patterns from an ontogenetic series of sheep molars (n = 45 M1s, 18 M2s). We adopt a Bayesian approach that posits a general pattern of maturation estimated from individual- and population-level mineral density variation over time. This approach converts static images of mineral density into a dynamic model of mineralization, and demonstrates that enamel secretion and maturation waves advance at nonlinear rates with distinct geometries. While enamel secretion is ordered, maturation geometry varies within a population and appears to be driven by diffusive processes. Our model yields concrete expectations for the integration of physiological and environmental signals, which is of particular significance for paleoseasonality research. This study also provides an avenue for characterizing mineralization patterns in other taxa. Our synchrotron imaging data and model are available for application to multiple disciplines, including health, material science, and paleontological research.</p></abstract><funding-group><award-group id="award001"><funding-source><institution>National Science Foundation</institution></funding-source><award-id>1247426</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-9817-541X</contrib-id><name><surname>Green</surname><given-names>Daniel R.</given-names></name></principal-award-recipient></award-group><award-group id="award002"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100005966</institution-id><institution>Leakey Foundation</institution></institution-wrap></funding-source><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-9817-541X</contrib-id><name><surname>Green</surname><given-names>Daniel R.</given-names></name></principal-award-recipient></award-group><award-group id="award003"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100001388</institution-id><institution>Wenner-Gren Foundation</institution></institution-wrap></funding-source><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-9817-541X</contrib-id><name><surname>Green</surname><given-names>Daniel R.</given-names></name></principal-award-recipient></award-group><award-group id="award004"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100001671</institution-id><institution>European Synchrotron Radiation Facility</institution></institution-wrap></funding-source><award-id>EC1018</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-9817-541X</contrib-id><name><surname>Green</surname><given-names>Daniel R.</given-names></name></principal-award-recipient></award-group><award-group id="award005"><funding-source><institution>National Science Foundation</institution></funding-source><award-id>0923831</award-id><principal-award-recipient><name><surname>Colman</surname><given-names>Albert S.</given-names></name></principal-award-recipient></award-group><funding-statement>This work was supported by National Science Foundation Grants 1247426 to DRG and 0923831 to ASC, the Wenner-Gren Foundation, the Leakey Foundation, Harvard University, and the European Synchrotron Radiation Facility award EC 1018 all to DRG.</funding-statement></funding-group><counts><fig-count count="8"></fig-count><table-count count="0"></table-count><page-count count="16"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>All relevant data are within the paper and its Supporting Information files.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>All relevant data are within the paper and its Supporting Information files.</p></notes></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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