Ten millennia of hepatitis B virus evolution

Author:

Kocher Arthur123ORCID,Papac Luka23ORCID,Barquera Rodrigo23ORCID,Key Felix M.24ORCID,Spyrou Maria A.235,Hübler Ron2ORCID,Rohrlach Adam B.236ORCID,Aron Franziska2ORCID,Stahl Raphaela2ORCID,Wissgott Antje2,van Bömmel Florian7ORCID,Pfefferkorn Maria7,Mittnik Alissa289ORCID,Villalba-Mouco Vanessa210ORCID,Neumann Gunnar U.23ORCID,Rivollat Maïté211ORCID,van de Loosdrecht Marieke S.2ORCID,Majander Kerttu212,Tukhbatova Rezeda I.213ORCID,Musralina Lyazzat231415ORCID,Ghalichi Ayshin23,Penske Sandra23ORCID,Sabin Susanna2ORCID,Michel Megan239ORCID,Gretzinger Joscha23,Nelson Elizabeth A.2ORCID,Ferraz Tiago216,Nägele Kathrin23ORCID,Parker Cody217ORCID,Keller Marcel218ORCID,Guevara Evelyn K.219ORCID,Feldman Michal25ORCID,Eisenmann Stefanie23ORCID,Skourtanioti Eirini23,Giffin Karen23ORCID,Gnecchi-Ruscone Guido Alberto23ORCID,Friederich Susanne20ORCID,Schimmenti Vittoria21,Khartanovich Valery22ORCID,Karapetian Marina K.23ORCID,Chaplygin Mikhail S.24ORCID,Kufterin Vladimir V.25ORCID,Khokhlov Aleksandr A.26ORCID,Chizhevsky Andrey A.27ORCID,Stashenkov Dmitry A.28ORCID,Kochkina Anna F.28,Tejedor-Rodríguez Cristina29ORCID,de Lagrán Íñigo García-Martínez30ORCID,Arcusa-Magallón Héctor31ORCID,Garrido-Pena Rafael32ORCID,Royo-Guillén José Ignacio33,Nováček Jan3435ORCID,Rottier Stéphane11ORCID,Kacki Sacha1136ORCID,Saintot Sylvie37ORCID,Kaverzneva Elena38ORCID,Belinskiy Andrej B.39,Velemínský Petr40ORCID,Limburský Petr41ORCID,Kostka Michal42ORCID,Loe Louise43,Popescu Elizabeth44,Clarke Rachel44,Lyons Alice44,Mortimer Richard44ORCID,Sajantila Antti1945ORCID,de Armas Yadira Chinique46ORCID,Hernandez Godoy Silvia Teresita4748ORCID,Hernández-Zaragoza Diana I.4950ORCID,Pearson Jessica51,Binder Didier52ORCID,Lefranc Philippe53,Kantorovich Anatoly R.54ORCID,Maslov Vladimir E.55ORCID,Lai Luca5657,Zoledziewska Magdalena58,Beckett Jessica F.59ORCID,Langová Michaela41ORCID,Danielisová Alžběta41ORCID,Ingman Tara60ORCID,Atiénzar Gabriel García61ORCID,de Miguel Ibáñez Maria Paz61ORCID,Romero Alejandro6162ORCID,Sperduti Alessandra6364ORCID,Beckett Sophie656667,Salter Susannah J.6568ORCID,Zilivinskaya Emma D.25,Vasil’ev Dmitry V.69ORCID,von Heyking Kristin70,Burger Richard L.71ORCID,Salazar Lucy C.71,Amkreutz Luc72ORCID,Navruzbekov Masnav73ORCID,Rosenstock Eva74ORCID,Alonso-Fernández Carmen75ORCID,Slavchev Vladimir76ORCID,Kalmykov Alexey A.39ORCID,Atabiev Biaslan Ch.77ORCID,Batieva Elena78ORCID,Calmet Micaela Alvarez79ORCID,Llamas Bastien808182ORCID,Schultz Michael8384,Krauß Raiko85ORCID,Jiménez-Echevarría Javier75ORCID,Francken Michael86ORCID,Shnaider Svetlana87ORCID,de Knijff Peter88ORCID,Altena Eveline88ORCID,Van de Vijver Katrien899091,Fehren-Schmitz Lars9293ORCID,Tung Tiffiny A.94ORCID,Lösch Sandra95ORCID,Dobrovolskaya Maria55,Makarov Nikolaj55,Read Chris96,Van Twest Melanie65ORCID,Sagona Claudia97ORCID,Ramsl Peter C.98ORCID,Akar Murat99ORCID,Yener K. Aslihan100ORCID,Ballestero Eduardo Carmona101102ORCID,Cucca Francesco58103ORCID,Mazzarello Vittorio103ORCID,Utrilla Pilar104,Rademaker Kurt105ORCID,Fernández-Domínguez Eva36ORCID,Baird Douglas51ORCID,Semal Patrick89ORCID,Márquez-Morfín Lourdes106ORCID,Roksandic Mirjana46107108ORCID,Steiner Hubert109ORCID,Salazar-García Domingo Carlos110111112,Shishlina Natalia2238ORCID,Erdal Yilmaz Selim113ORCID,Hallgren Fredrik114ORCID,Boyadzhiev Yavor115,Boyadzhiev Kamen115,Küßner Mario34ORCID,Sayer Duncan116ORCID,Onkamo Päivi117118ORCID,Skeates Robin36ORCID,Rojo-Guerra Manuel29ORCID,Buzhilova Alexandra23ORCID,Khussainova Elmira15ORCID,Djansugurova Leyla B.15ORCID,Beisenov Arman Z.119ORCID,Samashev Zainolla120121ORCID,Massy Ken122ORCID,Mannino Marcello123124ORCID,Moiseyev Vyacheslav22ORCID,Mannermaa Kristiina125,Balanovsky Oleg126127128,Deguilloux Marie-France11,Reinhold Sabine129ORCID,Hansen Svend129ORCID,Kitov Egor P.25119ORCID,Dobeš Miroslav41ORCID,Ernée Michal41ORCID,Meller Harald20ORCID,Alt Kurt W.130131132ORCID,Prüfer Kay23ORCID,Warinner Christina23133ORCID,Schiffels Stephan23ORCID,Stockhammer Philipp W.23122ORCID,Bos Kirsten23ORCID,Posth Cosimo25ORCID,Herbig Alexander23ORCID,Haak Wolfgang23134ORCID,Krause Johannes23ORCID,Kühnert Denise123135ORCID

Affiliation:

1. Transmission, Infection, Diversification and Evolution Group, Max Planck Institute for the Science of Human History, 07745 Jena, Germany.

2. Department of Archaeogenetics, Max Planck Institute for the Science of Human History, 07745 Jena, Germany.

3. Department of Archaeogenetics, Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany.

4. Max Planck Institute for Infection Biology, 10117 Berlin, Germany.

5. Archaeo- and Palaeogenetics group, Institute for Archaeological Sciences, Eberhard Karls University Tübingen, 72070 Tübingen, Germany.

6. ARC Centre of Excellence for Mathematical and Statistical Frontiers, School of Mathematical Sciences, University of Adelaide, Adelaide, SA 5005, Australia.

7. Division of Hepatology, Department of Medicine II, Leipzig University Medical Center, Leipzig, Germany.

8. Department of Genetics, Harvard Medical School, Boston, MA, USA.

9. Department of Human Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA.

10. Institute of Evolutionary Biology, CSIC-Universitat Pompeu Fabra, Barcelona, Spain.

11. Université de Bordeaux, CNRS, PACEA UMR 5199, Pessac, France.

12. Institute of Evolutionary Medicine (IEM), University of Zürich, 8057 Zürich, Switzerland.

13. Laboratory of Structural Biology, Kazan Federal University, Kazan, Russia.

14. Al-Farabi Kazakh National University, Almaty, Kazakhstan.

15. Institute of Genetics and Physiology, 050060 Almaty, Kazakhstan.

16. Departmento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Brazil.

17. Arizona State University School of Human Evolution and Social Change, Tempe Arizona, USA.

18. Estonian Biocentre, Institute of Genomics, University of Tartu, Tartu, Estonia.

19. Department of Forensic Medicine, University of Helsinki, Helsinki, Finland.

20. State Office for Heritage Management and Archaeology Saxony-Anhalt and State Museum of Prehistory, D-06114 Halle, Germany.

21. Museo Archeologico Regionale “Antonino Salinas”, 90133 Palermo, Italy.

22. Peter the Great Museum of Anthropology and Ethnography (Kunstkamera) RAS, 199034 St. Petersburg, Russia.

23. Anuchin Research Institute and Museum of Anthropology, Lomonosov Moscow State University, Moscow, Russia.

24. Sterlitamak Museum of Local History, Sterlitamak, Russia.

25. Institute of Ethnology and Anthropology, Russian Academy of Sciences, Moscow, Russia.

26. Samara State University of Social Sciences and Education, Samara, Russia.

27. Institute of Archaeology named after A. Kh. Khalikov, Tatarstan Academy of Sciences, Kazan, Russia.

28. Samara Museum for Historical and Regional Studies named after P. V. Alabin, Samara, Russia.

29. Department of Prehistory and Archaeology, Faculty of Philosophy and Letters, University of Valladolid, Spain.

30. Department of Prehistory and Archaeology, National Distance Education University (UNED), Madrid, Spain.

31. Private Technical Archaeologist, 50196 La Muela, Spain.

32. Department of Prehistory and Archaeology, Faculty of Philosophy and Letters, Autonomous University of Madrid, Spain.

33. Technical Archaeologist, Government of Aragón, Spain.

34. Thuringian State Office for Heritage Management and Archaeology, 99423 Weimar, Germany.

35. University Medical School Göttingen, Institute of Anatomy and Cell Biology, 37075 Göttingen, Germany.

36. Department of Archaeology, Durham University, South Road, Durham. DH1 3LE. UK.

37. INRAP, ARAR UMR 5138, Maison de l’Orient et de la Méditerranée, Lyon, France.

38. State Historical Museum, Moscow, Russia.

39. Nasledie Cultural Heritage Unit, 355006 Stavropol, Russia.

40. Department of Anthropology, The National Museum, Prague, Czech Republic.

41. Institute of Archaeology of the Czech Academy of Sciences, Prague, Czech Republic.

42. The City of Prague Museum, Prague, Czech Republic.

43. Oxford Archaeology South, Janus House, Osney Mead, Oxford, OX2 0ES, UK.

44. Oxford Archaeology East, Bar Hill, Cambridge, CB23 8SQ, UK.

45. Forensic Medicine Unit, Finnish Institute of Health and Welfare, Helsinki, Finland.

46. Department of Anthropology, University of Winnipeg, Winnipeg, MB, Canada.

47. Grupo de Investigación y Desarrollo, Dirección Provincial de Cultura, Matanzas, Cuba.

48. Universidad de Matanzas, Matanzas, Cuba.

49. Molecular Genetics Laboratory, Escuela Nacional de Antropología e Historia (ENAH), Mexico City, Mexico.

50. Immunogenetics Unit, Técnicas Genéticas Aplicadas a la Clínica (TGAC), Mexico City, Mexico.

51. Department of Archaeology, Classics and Egyptology, University of Liverpool, Liverpool L69 7WZ, UK.

52. Université Côte d’Azur, CNRS, CEPAM UMR 7264, Nice, France.

53. Université de Strasbourg, CNRS, Archimède UMR 7044, Strasbourg, France.

54. Department of Archaeology, Faculty of History, Lomonosov Moscow State University, 119192 Moscow, Russia.

55. Institute of Archaeology, Russian Academy of Sciences, , Moscow 117292, Russia.

56. Department of Anthropology, University of South Florida, Tampa, FL, USA.

57. Department of Anthropology, University of North Carolina at Charlotte, Charlotte, NC, USA.

58. Istituto di Ricerca Genetica e Biomedica–CNR, Monserrato, Italy.

59. Private contractor, Cagliari, Sardinia, Italy.

60. Koç University, Research Center for Anatolian Civilizations, Istanbul 34433, Turkey.

61. Institute for Research in Archaeology and Historical Heritage (INAPH), University of Alicante, 03690, Alicante, Spain.

62. Departamento de Biotecnología, Facultad de Ciencias, Universidad de Alicante, 03690, Alicante, Spain.

63. Bioarchaeology Service, Museum of Civilizations, Rome, Italy.

64. Dipartimento Asia Africa e Mediterraneo, Università di Napoli L’Orientale, Napoli, Italy.

65. Sedgeford Historical and Archaeological Research Project, Old Village Hall, Sedgeford, Hunstanton PE36 5LS, UK.

66. Melbourne Dental School, University of Melbourne, Victoria 3010 Australia.

67. Cranfield Forensic Institute, Cranfield Defence and Security, Cranfield University, College Road, Cranfield, MK43 0AL, UK.

68. Department of Veterinary Medicine, University of Cambridge, Cambridge CB3 0ES, UK.

69. Astrakhan State University, Astrakhan, Russia.

70. SNSB, State Collection for Anthropology and Palaeoanatomy, 80333 Munich, Germany.

71. Department of Anthropology, Yale University, New Haven, CT 06511, USA.

72. National Museum of Antiquities, 2301 EC Leiden, Netherlands.

73. Institute of History, Archaeology and Ethnography, Dushanbe, Tajikistan.

74. Freie Universität Berlin, Einstein Center Chronoi, 14195 Berlin, Germany.

75. Cronos S.C. Arqueología y Patrimonio, Burgos, Spain.

76. Regional Historical Museum Varna, Varna, BG-9000, Bulgaria.

77. Institute for Caucasus Archaeology, 361401 Nalchik, Republic Kabardino-Balkaria, Russia.

78. Azov History, Archaeology and Palaeontology Museum-Reserve, Azov 346780, Russia.

79. Museo de Sitio Pucllana, s/n Miraflores, 18 Lima, Peru.

80. Australian Centre for Ancient DNA, School of Biological Sciences and The Environment Institute, Adelaide University, Adelaide, SA 5005, Australia.

81. Centre of Excellence for Australian Biodiversity and Heritage (CABAH), University of Adelaide, Adelaide, SA 5005, Australia.

82. National Centre for Indigenous Genomics, Australian National University, Canberra, ACT 0200, Australia.

83. University Medical School Göttingen, Institute of Anatomy and Embryology, 37075 Göttingen, Germany.

84. Institute of Biology, University of Hildeshein, Germany.

85. Institute for Prehistory, Early History and Medieval Archaeology, University of Tübingen, 72070 Tübingen, Germany.

86. State Office for Cultural Heritage Baden-Württemberg, 78467 Konstanz, Germany.

87. ArchaeoZoology in Siberia and Central Asia–ZooSCAn, CNRS–IAET SB RAS International Research Laboratory, IRL 2013, Novosibirsk, Russia.

88. Department of Human Genetics, Leiden University Medical Center, Leiden, 2333 ZC, Netherlands.

89. Royal Belgian Institute of Natural Sciences, Brussels, Belgium.

90. Center for Archaeological Sciences, University of Leuven, Belgium.

91. Dienst Archeologie–Stad Mechelen, Belgium.

92. UCSC Paleogenomics Laboratory, Department of Anthropology, University of California at Santa Cruz, Santa Cruz, CA 95064, USA.

93. UCSC Genomics Institute, University of California at Santa Cruz, Santa Cruz, CA 95064, USA.

94. Department of Anthropology, Vanderbilt University, Nashville, TN 37235, USA.

95. Department of Physical Anthropology, Institute of Forensic Medicine, University of Bern, Bern, Switzerland.

96. Applied Archaeology School of Science, Institute of Technology Sligo, Ireland.

97. School of Historical and Philosophical Studies, University of Melbourne, Victoria 3010, Australia.

98. Institute of Prehistoric and Historical Archaeology, University of Vienna, Austria.

99. Department of Archaeology, Hatay Mustafa Kemal University, Alahan-Antakya, Hatay 31060, Turkey.

100. Institute for the Study of the Ancient World (ISAW), New York University, New York, NY 10028, USA.

101. Territorial Service of Culture and Tourism from Valladolid, Castilla y León Regional Government, C/ San Lorenzo, 5, 47001, Valladolid, Spain.

102. Department of History, Geography and Comunication, University of Burgos, Paseo de Comendadores, s/n 09001 Burgos (Burgos), Spain.

103. Dipartimento di Scienze Biomediche, Università di Sassari, Sassari, Italy.

104. Área de Prehistoria, P3A DGA Research Group, IPH, University of Zaragoza, C/ Pedro Cerbuna 12, 50009, Zaragoza, Spain.

105. Department of Anthropology, Michigan State University, East Lansing, MI 48824, USA.

106. Osteology Laboratory, Post Graduate Studies Division, Escuela Nacional de Antropología e Historia (ENAH), Mexico City, Mexico.

107. Caribbean Research Institute, Univeristy of Winnipeg, Winnipeg, MB, Canada.

108. DFG Center for Advanced Studies “Words, Bones, Genes, Tools,” University of Tübingen, Tübingen, Germany.

109. South Tyrol Provincial Heritage Service, South Tyrol, Italy.

110. Grupo de Investigación en Prehistoria IT-1223-19 (UPV-EHU)/IKERBASQUE-Basque Foundation for Science, Vitoria, Spain.

111. Departament de Prehistòria, Arqueologia i Història Antiga, Universitat de València, València, Spain.

112. Department of Geological Sciences, University of Cape Town, Cape Town, South Africa.

113. Human_G Laboratory, Department of Anthropology, Hacettepe University, Ankara 06800, Turkey.

114. The Cultural Heritage Foundation, 722 12 Västerås, Sweden.

115. National Archaeological Institute with Museum at the Bulgarian Academy of Sciences, Sofia 1000, Bulgaria.

116. School of Natural Sciences, University of Central Lancashire, Preston, UK.

117. Department of Biosciences, University of Helsinki, 00014 Helsinki, Finland.

118. Department of Biology, University of Turku, 20500 Turku, Finland.

119. Institute of archaeology named after A. Kh. Margulan, 44 Almaty, Kazakhstan.

120. Branch of Institute of Archaeology named after A.Kh. Margulan, 24 of 511 Nur-Sultan, Kazakhstan.

121. State Historical and Cultural Museum-Reserve “Berel,” Katon-Karagay district, East Kazakhstan region, Kazakhstan.

122. Institut für Vor- und Frühgeschichtliche Archäologie und Provinzialrömische Archäologie, Ludwig-Maximilians-Universität München, 80539 Munich, Germany.

123. Department of Archeology and Heritage Studies, Aarhus University, 8270 Højbjerg, Denmark.

124. Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig Germany.

125. Department of Cultures, University of Helsinki, 00014 Helsinki, Finland.

126. Research Centre for Medical Genetics, Moscow, Russia.

127. Biobank of North Eurasia, Moscow, Russia.

128. Vavilov Institute of General Genetics, Moscow, Russia.

129. Eurasia Department, German Archaeological Institute, Berlin, Germany.

130. Danube Private University, Center of Natural and Cultural Human History, A - 3500 Krems-Stein, Austria.

131. Integrative Prehistory and Archaeological Science, Spalenring 145, CH-4055 Basel, Switzerland.

132. Department of Biomedical Engineering (DBE), Universitätsspital Basel (HFZ), CH-4123 Allschwil, Switzerland.

133. Department of Anthropology, Harvard University, Cambridge, MA 02138, USA.

134. School of Biological Sciences, University of Adelaide, Adelaide, SA, 5005, Australia.

135. European Virus Bioinformatics Center (EVBC), Jena, Germany.

Abstract

Ancient DNA traces the history of hepatitis B Hepatitis B virus (HBV) infections represent a worldwide human health concern. To study the history of this pathogen, Kocher et al . identified 137 human remains with detectable levels of virus dating between 400 and 10,000 years ago. Sequencing and analyses of these ancient viruses suggested a common ancestor between 12,000 and 20,000 years ago. There is no evidence indicating that HBV was present in the earliest humans as they spread out of Africa; however, HBV was likely present in human populations before farming. Furthermore, the virus was present in the Americas by about 9000 years ago, representing a lineage sister to the viral strains found in Eurasia that diverged about 20,000 years ago. —LMZ

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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