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17th Century Variola Virus Reveals the Recent History of Smallpox

Identifieur interne : 002541 ( Main/Exploration ); précédent : 002540; suivant : 002542

17th Century Variola Virus Reveals the Recent History of Smallpox

Auteurs : Ana T. Duggan [Canada] ; Maria F. Perdomo [Finlande] ; Dario Piombino-Mascali [Lituanie] ; Stephanie Marciniak [Canada] ; Debi Poinar [Canada] ; Matthew V. Emery [Canada] ; Jan P. Buchmann [Australie] ; Sebastian Duchêne [Australie] ; Rimantas Jankauskas [Lituanie] ; Margaret Humphreys [États-Unis] ; G. Brian Golding [Canada] ; John Southon [États-Unis] ; Alison Devault [États-Unis] ; Jean-Marie Rouillard [États-Unis] ; Jason W. Sahl [États-Unis] ; Olivier Dutour [France] ; Klaus Hedman [Finlande] ; Antti Sajantila [Finlande] ; Geoffrey L. Smith [Royaume-Uni] ; Edward C. Holmes [Australie] ; Hendrik N. Poinar [Canada]

Source :

RBID : PMC:5196022

Abstract

Summary

Smallpox holds a unique position in the history of medicine. It was the first disease for which a vaccine was developed and remains the only human disease eradicated by vaccination. Although there have been claims of smallpox in Egypt, India, and China dating back millennia [1, 2, 3, 4], the timescale of emergence of the causative agent, variola virus (VARV), and how it evolved in the context of increasingly widespread immunization, have proven controversial [4, 5, 6, 7, 8, 9]. In particular, some molecular-clock-based studies have suggested that key events in VARV evolution only occurred during the last two centuries [4, 5, 6] and hence in apparent conflict with anecdotal historical reports, although it is difficult to distinguish smallpox from other pustular rashes by description alone. To address these issues, we captured, sequenced, and reconstructed a draft genome of an ancient strain of VARV, sampled from a Lithuanian child mummy dating between 1643 and 1665 and close to the time of several documented European epidemics [1, 2, 10]. When compared to vaccinia virus, this archival strain contained the same pattern of gene degradation as 20th century VARVs, indicating that such loss of gene function had occurred before ca. 1650. Strikingly, the mummy sequence fell basal to all currently sequenced strains of VARV on phylogenetic trees. Molecular-clock analyses revealed a strong clock-like structure and that the timescale of smallpox evolution is more recent than often supposed, with the diversification of major viral lineages only occurring within the 18th and 19th centuries, concomitant with the development of modern vaccination.


Url:
DOI: 10.1016/j.cub.2016.10.061
PubMed: 27939314
PubMed Central: 5196022


Affiliations:


Links toward previous steps (curation, corpus...)


Le document en format XML

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Century Variola Virus Reveals the Recent History of Smallpox</title>
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<name sortKey="Sajantila, Antti" sort="Sajantila, Antti" uniqKey="Sajantila A" first="Antti" last="Sajantila">Antti Sajantila</name>
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<nlm:aff id="aff17">Michael G. DeGroote Institute for Infectious Disease Research, McMaster University, Hamilton, ON L8S 4L8, Canada</nlm:aff>
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<title xml:lang="en" level="a" type="main">17
<sup>th</sup>
Century Variola Virus Reveals the Recent History of Smallpox</title>
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<name sortKey="Duggan, Ana T" sort="Duggan, Ana T" uniqKey="Duggan A" first="Ana T." last="Duggan">Ana T. Duggan</name>
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<name sortKey="Perdomo, Maria F" sort="Perdomo, Maria F" uniqKey="Perdomo M" first="Maria F." last="Perdomo">Maria F. Perdomo</name>
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<name sortKey="Piombino Mascali, Dario" sort="Piombino Mascali, Dario" uniqKey="Piombino Mascali D" first="Dario" last="Piombino-Mascali">Dario Piombino-Mascali</name>
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<nlm:aff id="aff3">Department of Anatomy, Histology, and Anthropology, Faculty of Medicine, Vilnius University, Vilnius 03101, Lithuania</nlm:aff>
<country xml:lang="fr">Lituanie</country>
<wicri:regionArea>Department of Anatomy, Histology, and Anthropology, Faculty of Medicine, Vilnius University, Vilnius 03101</wicri:regionArea>
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</affiliation>
</author>
<author>
<name sortKey="Marciniak, Stephanie" sort="Marciniak, Stephanie" uniqKey="Marciniak S" first="Stephanie" last="Marciniak">Stephanie Marciniak</name>
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<nlm:aff id="aff1">McMaster Ancient DNA Centre, Department of Anthropology, McMaster University, Hamilton, ON L8S 4L8, Canada</nlm:aff>
<country xml:lang="fr">Canada</country>
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<orgName type="university">Université McMaster</orgName>
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<settlement type="city">Hamilton (Ontario)</settlement>
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</affiliation>
</author>
<author>
<name sortKey="Poinar, Debi" sort="Poinar, Debi" uniqKey="Poinar D" first="Debi" last="Poinar">Debi Poinar</name>
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<nlm:aff id="aff1">McMaster Ancient DNA Centre, Department of Anthropology, McMaster University, Hamilton, ON L8S 4L8, Canada</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea>McMaster Ancient DNA Centre, Department of Anthropology, McMaster University, Hamilton, ON L8S 4L8</wicri:regionArea>
<orgName type="university">Université McMaster</orgName>
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<settlement type="city">Hamilton (Ontario)</settlement>
<region type="state">Ontario</region>
</placeName>
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</author>
<author>
<name sortKey="Emery, Matthew V" sort="Emery, Matthew V" uniqKey="Emery M" first="Matthew V." last="Emery">Matthew V. Emery</name>
<affiliation wicri:level="4">
<nlm:aff id="aff1">McMaster Ancient DNA Centre, Department of Anthropology, McMaster University, Hamilton, ON L8S 4L8, Canada</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea>McMaster Ancient DNA Centre, Department of Anthropology, McMaster University, Hamilton, ON L8S 4L8</wicri:regionArea>
<orgName type="university">Université McMaster</orgName>
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<settlement type="city">Hamilton (Ontario)</settlement>
<region type="state">Ontario</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Buchmann, Jan P" sort="Buchmann, Jan P" uniqKey="Buchmann J" first="Jan P." last="Buchmann">Jan P. Buchmann</name>
<affiliation wicri:level="4">
<nlm:aff id="aff4">Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, NSW 2145, Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, NSW 2145</wicri:regionArea>
<orgName type="university">Université de Sydney</orgName>
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<settlement type="city">Sydney</settlement>
<region type="état">Nouvelle-Galles du Sud</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Duchene, Sebastian" sort="Duchene, Sebastian" uniqKey="Duchene S" first="Sebastian" last="Duchêne">Sebastian Duchêne</name>
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<nlm:aff id="aff4">Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, NSW 2145, Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, NSW 2145</wicri:regionArea>
<orgName type="university">Université de Sydney</orgName>
<placeName>
<settlement type="city">Sydney</settlement>
<region type="état">Nouvelle-Galles du Sud</region>
</placeName>
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<affiliation wicri:level="4">
<nlm:aff id="aff5">Department of Biochemistry and Molecular Biology, Bio21 Molecular Science and Biotechnology Institute, The University of Melbourne, Melbourne, VIC 3010, Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Department of Biochemistry and Molecular Biology, Bio21 Molecular Science and Biotechnology Institute, The University of Melbourne, Melbourne, VIC 3010</wicri:regionArea>
<orgName type="university">Université de Melbourne</orgName>
<placeName>
<settlement type="city">Melbourne</settlement>
<region type="état">Victoria (État)</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Jankauskas, Rimantas" sort="Jankauskas, Rimantas" uniqKey="Jankauskas R" first="Rimantas" last="Jankauskas">Rimantas Jankauskas</name>
<affiliation wicri:level="1">
<nlm:aff id="aff3">Department of Anatomy, Histology, and Anthropology, Faculty of Medicine, Vilnius University, Vilnius 03101, Lithuania</nlm:aff>
<country xml:lang="fr">Lituanie</country>
<wicri:regionArea>Department of Anatomy, Histology, and Anthropology, Faculty of Medicine, Vilnius University, Vilnius 03101</wicri:regionArea>
<wicri:noRegion>Vilnius 03101</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Humphreys, Margaret" sort="Humphreys, Margaret" uniqKey="Humphreys M" first="Margaret" last="Humphreys">Margaret Humphreys</name>
<affiliation wicri:level="2">
<nlm:aff id="aff6">Department of History, Duke University, Durham, NC 27708-0719, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of History, Duke University, Durham, NC 27708-0719</wicri:regionArea>
<placeName>
<region type="state">Caroline du Nord</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Golding, G Brian" sort="Golding, G Brian" uniqKey="Golding G" first="G. Brian" last="Golding">G. Brian Golding</name>
<affiliation wicri:level="4">
<nlm:aff id="aff7">Department of Biology, McMaster University, Hamilton, ON L8S 4L8, Canada</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea>Department of Biology, McMaster University, Hamilton, ON L8S 4L8</wicri:regionArea>
<orgName type="university">Université McMaster</orgName>
<placeName>
<settlement type="city">Hamilton (Ontario)</settlement>
<region type="state">Ontario</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Southon, John" sort="Southon, John" uniqKey="Southon J" first="John" last="Southon">John Southon</name>
<affiliation wicri:level="2">
<nlm:aff id="aff8">Keck Carbon Cycle Accelerator Mass Spectrometer, Earth Systems Science Department, University of California, Irvine, CA 92697-3100, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Keck Carbon Cycle Accelerator Mass Spectrometer, Earth Systems Science Department, University of California, Irvine, CA 92697-3100</wicri:regionArea>
<placeName>
<region type="state">Californie</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Devault, Alison" sort="Devault, Alison" uniqKey="Devault A" first="Alison" last="Devault">Alison Devault</name>
<affiliation wicri:level="2">
<nlm:aff id="aff9">MYcroarray, Ann Arbor, MI 48105, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>MYcroarray, Ann Arbor, MI 48105</wicri:regionArea>
<placeName>
<region type="state">Michigan</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Rouillard, Jean Marie" sort="Rouillard, Jean Marie" uniqKey="Rouillard J" first="Jean-Marie" last="Rouillard">Jean-Marie Rouillard</name>
<affiliation wicri:level="2">
<nlm:aff id="aff9">MYcroarray, Ann Arbor, MI 48105, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>MYcroarray, Ann Arbor, MI 48105</wicri:regionArea>
<placeName>
<region type="state">Michigan</region>
</placeName>
</affiliation>
<affiliation wicri:level="2">
<nlm:aff id="aff10">Department of Chemical Engineering, University of Michigan, Ann Arbor, MI 48109-2136, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Chemical Engineering, University of Michigan, Ann Arbor, MI 48109-2136</wicri:regionArea>
<placeName>
<region type="state">Michigan</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Sahl, Jason W" sort="Sahl, Jason W" uniqKey="Sahl J" first="Jason W." last="Sahl">Jason W. Sahl</name>
<affiliation wicri:level="2">
<nlm:aff id="aff11">Center for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, AZ 86011-4073, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Center for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, AZ 86011-4073</wicri:regionArea>
<placeName>
<region type="state">Arizona</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Dutour, Olivier" sort="Dutour, Olivier" uniqKey="Dutour O" first="Olivier" last="Dutour">Olivier Dutour</name>
<affiliation wicri:level="3">
<nlm:aff id="aff12">Laboratoire d’Anthropologie Biologique Paul Broca, Ecole Pratique des Hautes Etudes, PSL Research University, Paris 75014, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Laboratoire d’Anthropologie Biologique Paul Broca, Ecole Pratique des Hautes Etudes, PSL Research University, Paris 75014</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Île-de-France</region>
</placeName>
</affiliation>
<affiliation wicri:level="4">
<nlm:aff id="aff13">PACEA, CNRS, Université de Bordeaux, Pessac 33615, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>PACEA, CNRS, Université de Bordeaux, Pessac 33615</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Nouvelle-Aquitaine</region>
<region type="old region" nuts="2">Aquitaine</region>
<settlement type="city">Bordeaux</settlement>
</placeName>
<orgName type="university">Université de Bordeaux</orgName>
</affiliation>
</author>
<author>
<name sortKey="Hedman, Klaus" sort="Hedman, Klaus" uniqKey="Hedman K" first="Klaus" last="Hedman">Klaus Hedman</name>
<affiliation wicri:level="4">
<nlm:aff id="aff2">Department of Virology, University of Helsinki, Helsinki 00014, Finland</nlm:aff>
<country xml:lang="fr">Finlande</country>
<wicri:regionArea>Department of Virology, University of Helsinki, Helsinki 00014</wicri:regionArea>
<orgName type="university">Université d'Helsinki</orgName>
<placeName>
<settlement type="city">Helsinki</settlement>
<region type="région" nuts="2">Uusimaa</region>
</placeName>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="aff14">Helsinki University Hospital, Helsinki 00029, Finland</nlm:aff>
<country xml:lang="fr">Finlande</country>
<wicri:regionArea>Helsinki University Hospital, Helsinki 00029</wicri:regionArea>
<wicri:noRegion>Helsinki 00029</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Sajantila, Antti" sort="Sajantila, Antti" uniqKey="Sajantila A" first="Antti" last="Sajantila">Antti Sajantila</name>
<affiliation wicri:level="4">
<nlm:aff id="aff15">Department of Forensic Medicine, University of Helsinki, Helsinki 00014, Finland</nlm:aff>
<country xml:lang="fr">Finlande</country>
<wicri:regionArea>Department of Forensic Medicine, University of Helsinki, Helsinki 00014</wicri:regionArea>
<orgName type="university">Université d'Helsinki</orgName>
<placeName>
<settlement type="city">Helsinki</settlement>
<region type="région" nuts="2">Uusimaa</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Smith, Geoffrey L" sort="Smith, Geoffrey L" uniqKey="Smith G" first="Geoffrey L." last="Smith">Geoffrey L. Smith</name>
<affiliation wicri:level="4">
<nlm:aff id="aff16">Department of Pathology, University of Cambridge, Cambridge CB2 1QP, UK</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>Department of Pathology, University of Cambridge, Cambridge CB2 1QP</wicri:regionArea>
<orgName type="university">Université de Cambridge</orgName>
<placeName>
<settlement type="city">Cambridge</settlement>
<region type="country">Angleterre</region>
<region type="région" nuts="1">Angleterre de l'Est</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Holmes, Edward C" sort="Holmes, Edward C" uniqKey="Holmes E" first="Edward C." last="Holmes">Edward C. Holmes</name>
<affiliation wicri:level="4">
<nlm:aff id="aff4">Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, NSW 2145, Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, NSW 2145</wicri:regionArea>
<orgName type="university">Université de Sydney</orgName>
<placeName>
<settlement type="city">Sydney</settlement>
<region type="état">Nouvelle-Galles du Sud</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Poinar, Hendrik N" sort="Poinar, Hendrik N" uniqKey="Poinar H" first="Hendrik N." last="Poinar">Hendrik N. Poinar</name>
<affiliation wicri:level="4">
<nlm:aff id="aff1">McMaster Ancient DNA Centre, Department of Anthropology, McMaster University, Hamilton, ON L8S 4L8, Canada</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea>McMaster Ancient DNA Centre, Department of Anthropology, McMaster University, Hamilton, ON L8S 4L8</wicri:regionArea>
<orgName type="university">Université McMaster</orgName>
<placeName>
<settlement type="city">Hamilton (Ontario)</settlement>
<region type="state">Ontario</region>
</placeName>
</affiliation>
<affiliation wicri:level="4">
<nlm:aff id="aff7">Department of Biology, McMaster University, Hamilton, ON L8S 4L8, Canada</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea>Department of Biology, McMaster University, Hamilton, ON L8S 4L8</wicri:regionArea>
<orgName type="university">Université McMaster</orgName>
<placeName>
<settlement type="city">Hamilton (Ontario)</settlement>
<region type="state">Ontario</region>
</placeName>
</affiliation>
<affiliation wicri:level="4">
<nlm:aff id="aff17">Michael G. DeGroote Institute for Infectious Disease Research, McMaster University, Hamilton, ON L8S 4L8, Canada</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea>Michael G. DeGroote Institute for Infectious Disease Research, McMaster University, Hamilton, ON L8S 4L8</wicri:regionArea>
<orgName type="university">Université McMaster</orgName>
<placeName>
<settlement type="city">Hamilton (Ontario)</settlement>
<region type="state">Ontario</region>
</placeName>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="aff18">Humans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1Z8, Canada</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea>Humans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1Z8</wicri:regionArea>
<wicri:noRegion>ON M5G 1Z8</wicri:noRegion>
</affiliation>
</author>
</analytic>
<series>
<title level="j">Current Biology</title>
<idno type="ISSN">0960-9822</idno>
<idno type="eISSN">1879-0445</idno>
<imprint>
<date when="2016">2016</date>
</imprint>
</series>
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<textClass></textClass>
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<front>
<div type="abstract" xml:lang="en">
<title>Summary</title>
<p>Smallpox holds a unique position in the history of medicine. It was the first disease for which a vaccine was developed and remains the only human disease eradicated by vaccination. Although there have been claims of smallpox in Egypt, India, and China dating back millennia [
<xref rid="bib1" ref-type="bibr">1</xref>
,
<xref rid="bib2" ref-type="bibr">2</xref>
,
<xref rid="bib3" ref-type="bibr">3</xref>
,
<xref rid="bib4" ref-type="bibr">4</xref>
], the timescale of emergence of the causative agent, variola virus (VARV), and how it evolved in the context of increasingly widespread immunization, have proven controversial [
<xref rid="bib4" ref-type="bibr">4</xref>
,
<xref rid="bib5" ref-type="bibr">5</xref>
,
<xref rid="bib6" ref-type="bibr">6</xref>
,
<xref rid="bib7" ref-type="bibr">7</xref>
,
<xref rid="bib8" ref-type="bibr">8</xref>
,
<xref rid="bib9" ref-type="bibr">9</xref>
]. In particular, some molecular-clock-based studies have suggested that key events in VARV evolution only occurred during the last two centuries [
<xref rid="bib4" ref-type="bibr">4</xref>
,
<xref rid="bib5" ref-type="bibr">5</xref>
,
<xref rid="bib6" ref-type="bibr">6</xref>
] and hence in apparent conflict with anecdotal historical reports, although it is difficult to distinguish smallpox from other pustular rashes by description alone. To address these issues, we captured, sequenced, and reconstructed a draft genome of an ancient strain of VARV, sampled from a Lithuanian child mummy dating between 1643 and 1665 and close to the time of several documented European epidemics [
<xref rid="bib1" ref-type="bibr">1</xref>
,
<xref rid="bib2" ref-type="bibr">2</xref>
,
<xref rid="bib10" ref-type="bibr">10</xref>
]. When compared to vaccinia virus, this archival strain contained the same pattern of gene degradation as 20
<sup>th</sup>
century VARVs, indicating that such loss of gene function had occurred before ca. 1650. Strikingly, the mummy sequence fell basal to all currently sequenced strains of VARV on phylogenetic trees. Molecular-clock analyses revealed a strong clock-like structure and that the timescale of smallpox evolution is more recent than often supposed, with the diversification of major viral lineages only occurring within the 18
<sup>th</sup>
and 19
<sup>th</sup>
centuries, concomitant with the development of modern vaccination.</p>
</div>
</front>
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<name sortKey="Selmes, I P" uniqKey="Selmes I">I.P. Selmes</name>
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<biblStruct>
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</analytic>
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<biblStruct>
<analytic>
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<name sortKey="Silverstein, A M" uniqKey="Silverstein A">A.M. Silverstein</name>
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</listBibl>
</div1>
</back>
</TEI>
<affiliations>
<list>
<country>
<li>Australie</li>
<li>Canada</li>
<li>Finlande</li>
<li>France</li>
<li>Lituanie</li>
<li>Royaume-Uni</li>
<li>États-Unis</li>
</country>
<region>
<li>Angleterre</li>
<li>Angleterre de l'Est</li>
<li>Aquitaine</li>
<li>Arizona</li>
<li>Californie</li>
<li>Caroline du Nord</li>
<li>Michigan</li>
<li>Nouvelle-Aquitaine</li>
<li>Nouvelle-Galles du Sud</li>
<li>Ontario</li>
<li>Uusimaa</li>
<li>Victoria (État)</li>
<li>Île-de-France</li>
</region>
<settlement>
<li>Bordeaux</li>
<li>Cambridge</li>
<li>Hamilton (Ontario)</li>
<li>Helsinki</li>
<li>Melbourne</li>
<li>Sydney</li>
</settlement>
<orgName>
<li>Université McMaster</li>
<li>Université d'Helsinki</li>
<li>Université de Bordeaux</li>
<li>Université de Cambridge</li>
<li>Université de Melbourne</li>
<li>Université de Sydney</li>
</orgName>
</list>
<tree>
<country name="Canada">
<region name="Ontario">
<name sortKey="Duggan, Ana T" sort="Duggan, Ana T" uniqKey="Duggan A" first="Ana T." last="Duggan">Ana T. Duggan</name>
</region>
<name sortKey="Emery, Matthew V" sort="Emery, Matthew V" uniqKey="Emery M" first="Matthew V." last="Emery">Matthew V. Emery</name>
<name sortKey="Golding, G Brian" sort="Golding, G Brian" uniqKey="Golding G" first="G. Brian" last="Golding">G. Brian Golding</name>
<name sortKey="Marciniak, Stephanie" sort="Marciniak, Stephanie" uniqKey="Marciniak S" first="Stephanie" last="Marciniak">Stephanie Marciniak</name>
<name sortKey="Poinar, Debi" sort="Poinar, Debi" uniqKey="Poinar D" first="Debi" last="Poinar">Debi Poinar</name>
<name sortKey="Poinar, Hendrik N" sort="Poinar, Hendrik N" uniqKey="Poinar H" first="Hendrik N." last="Poinar">Hendrik N. Poinar</name>
<name sortKey="Poinar, Hendrik N" sort="Poinar, Hendrik N" uniqKey="Poinar H" first="Hendrik N." last="Poinar">Hendrik N. Poinar</name>
<name sortKey="Poinar, Hendrik N" sort="Poinar, Hendrik N" uniqKey="Poinar H" first="Hendrik N." last="Poinar">Hendrik N. Poinar</name>
<name sortKey="Poinar, Hendrik N" sort="Poinar, Hendrik N" uniqKey="Poinar H" first="Hendrik N." last="Poinar">Hendrik N. Poinar</name>
</country>
<country name="Finlande">
<region name="Uusimaa">
<name sortKey="Perdomo, Maria F" sort="Perdomo, Maria F" uniqKey="Perdomo M" first="Maria F." last="Perdomo">Maria F. Perdomo</name>
</region>
<name sortKey="Hedman, Klaus" sort="Hedman, Klaus" uniqKey="Hedman K" first="Klaus" last="Hedman">Klaus Hedman</name>
<name sortKey="Hedman, Klaus" sort="Hedman, Klaus" uniqKey="Hedman K" first="Klaus" last="Hedman">Klaus Hedman</name>
<name sortKey="Sajantila, Antti" sort="Sajantila, Antti" uniqKey="Sajantila A" first="Antti" last="Sajantila">Antti Sajantila</name>
</country>
<country name="Lituanie">
<noRegion>
<name sortKey="Piombino Mascali, Dario" sort="Piombino Mascali, Dario" uniqKey="Piombino Mascali D" first="Dario" last="Piombino-Mascali">Dario Piombino-Mascali</name>
</noRegion>
<name sortKey="Jankauskas, Rimantas" sort="Jankauskas, Rimantas" uniqKey="Jankauskas R" first="Rimantas" last="Jankauskas">Rimantas Jankauskas</name>
</country>
<country name="Australie">
<region name="Nouvelle-Galles du Sud">
<name sortKey="Buchmann, Jan P" sort="Buchmann, Jan P" uniqKey="Buchmann J" first="Jan P." last="Buchmann">Jan P. Buchmann</name>
</region>
<name sortKey="Duchene, Sebastian" sort="Duchene, Sebastian" uniqKey="Duchene S" first="Sebastian" last="Duchêne">Sebastian Duchêne</name>
<name sortKey="Duchene, Sebastian" sort="Duchene, Sebastian" uniqKey="Duchene S" first="Sebastian" last="Duchêne">Sebastian Duchêne</name>
<name sortKey="Holmes, Edward C" sort="Holmes, Edward C" uniqKey="Holmes E" first="Edward C." last="Holmes">Edward C. Holmes</name>
</country>
<country name="États-Unis">
<region name="Caroline du Nord">
<name sortKey="Humphreys, Margaret" sort="Humphreys, Margaret" uniqKey="Humphreys M" first="Margaret" last="Humphreys">Margaret Humphreys</name>
</region>
<name sortKey="Devault, Alison" sort="Devault, Alison" uniqKey="Devault A" first="Alison" last="Devault">Alison Devault</name>
<name sortKey="Rouillard, Jean Marie" sort="Rouillard, Jean Marie" uniqKey="Rouillard J" first="Jean-Marie" last="Rouillard">Jean-Marie Rouillard</name>
<name sortKey="Rouillard, Jean Marie" sort="Rouillard, Jean Marie" uniqKey="Rouillard J" first="Jean-Marie" last="Rouillard">Jean-Marie Rouillard</name>
<name sortKey="Sahl, Jason W" sort="Sahl, Jason W" uniqKey="Sahl J" first="Jason W." last="Sahl">Jason W. Sahl</name>
<name sortKey="Southon, John" sort="Southon, John" uniqKey="Southon J" first="John" last="Southon">John Southon</name>
</country>
<country name="France">
<region name="Île-de-France">
<name sortKey="Dutour, Olivier" sort="Dutour, Olivier" uniqKey="Dutour O" first="Olivier" last="Dutour">Olivier Dutour</name>
</region>
<name sortKey="Dutour, Olivier" sort="Dutour, Olivier" uniqKey="Dutour O" first="Olivier" last="Dutour">Olivier Dutour</name>
</country>
<country name="Royaume-Uni">
<region name="Angleterre">
<name sortKey="Smith, Geoffrey L" sort="Smith, Geoffrey L" uniqKey="Smith G" first="Geoffrey L." last="Smith">Geoffrey L. Smith</name>
</region>
</country>
</tree>
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</record>

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