1887

Abstract

The genus includes some of the most important human viral pathogens, and its members are found in all parts of the populated world. The temporal origin of diversification of the genus has long been debated due to the inherent problems with dating deep RNA virus evolution. A generally accepted hypothesis suggests that emerged within the last 10 000 years. However, it has been argued that the tick-borne Powassan flavivirus was introduced into North America some time between the opening and closing of the Beringian land bridge that connected Asia and North America 15 000–11 000 years ago, indicating an even older origin for . To determine the temporal origin of , we performed Bayesian relaxed molecular clock dating on a dataset with high coverage of the presently available diversity by combining tip date calibrations and internal node calibration, based on the Powassan virus and Beringian land bridge biogeographical event. Our analysis suggested that originated ~85 000 (64 000–110 000) or 120 000 (87 000–159 000) years ago, depending on the circumscription of the genus. This is significantly older than estimated previously. In light of our results, we propose that it is likely that modern humans came in contact with several members of the genus much earlier than suggested previously, and that it is possible that the spread of several flaviviruses coincided with, and was facilitated by, the migration and population expansion of modern humans out of Africa.

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2014-09-01
2024-12-10
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References

  1. Achilli A., Perego U. A., Lancioni H., Olivieri A., Gandini F., Hooshiar Kashani B., Battaglia V., Grugni V., Angerhofer N.other authors 2013; Reconciling migration models to the Americas with the variation of North American native mitogenomes. Proc Natl Acad Sci U S A 110:14308–14313 [View Article][PubMed]
    [Google Scholar]
  2. Bertrand Y., Töpel M., Elväng A., Melik W., Johansson M. 2012; First dating of a recombination event in mammalian tick-borne flaviviruses. PLoS ONE 7:e31981 [View Article][PubMed]
    [Google Scholar]
  3. Billoir F., de Chesse R., Tolou H., de Micco P., Gould E. A., de Lamballerie X. 2000; Phylogeny of the genus flavivirus using complete coding sequences of arthropod-borne viruses and viruses with no known vector. J Gen Virol 81:781–790[PubMed]
    [Google Scholar]
  4. Blome M. W., Cohen A. S., Tryon C. A., Brooks A. S., Russell J. 2012; The environmental context for the origins of modern human diversity: a synthesis of regional variability in African climate 150,000–30,000 years ago. J Hum Evol 62:563–592 [View Article][PubMed]
    [Google Scholar]
  5. Bodner M., Perego U. A., Huber G., Fendt L., Röck A. W., Zimmermann B., Olivieri A., Gómez-Carballa A., Lancioni H.other authors 2012; Rapid coastal spread of First Americans: novel insights from South America’s Southern Cone mitochondrial genomes. Genome Res 22:811–820 [View Article][PubMed]
    [Google Scholar]
  6. Bolling B. G., Olea-Popelka F. J., Eisen L., Moore C. G., Blair C. D. 2012; Transmission dynamics of an insect-specific flavivirus in a naturally infected Culex pipiens laboratory colony and effects of co-infection on vector competence for West Nile virus. Virology 427:90–97 [View Article][PubMed]
    [Google Scholar]
  7. Bromham L., Penny D. 2003; The modern molecular clock. Nat Rev Genet 4:216–224 [View Article][PubMed]
    [Google Scholar]
  8. Catto N. R. 1996; Richardson Mountains, Yukon-Northwest territories: the northern portal of the postulated ‘Ice-Free Corridor’. Quartern Int 32:3–19 [View Article]
    [Google Scholar]
  9. Cavalli-Sforza L. L., Feldman M. W. 2003; The application of molecular genetic approaches to the study of human evolution. Nat Genet 33:Suppl266–275 [View Article][PubMed]
    [Google Scholar]
  10. Chambers T. J., Hahn C. S., Galler R., Rice C. M. 1990; Flavivirus genome organization, expression, and replication. Annu Rev Microbiol 44:649–688 [View Article][PubMed]
    [Google Scholar]
  11. Comas I., Coscolla M., Luo T., Borrell S., Holt K. E., Kato-Maeda M., Parkhill J., Malla B., Berg S.other authors 2013; Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat Genet 45:1176–1182 [View Article][PubMed]
    [Google Scholar]
  12. Cook S., Holmes E. C. 2006; A multigene analysis of the phylogenetic relationships among the flaviviruses (Family: Flaviviridae) and the evolution of vector transmission. Arch Virol 151:309–325 [View Article][PubMed]
    [Google Scholar]
  13. Cook S., Moureau G., Kitchen A., Gould E. A., de Lamballerie X., Holmes E. C., Harbach R. E. 2012; Molecular evolution of the insect-specific flaviviruses. J Gen Virol 93:223–234 [View Article][PubMed]
    [Google Scholar]
  14. Crochu S., Cook S., Attoui H., Charrel R. N., De Chesse R., Belhouchet M., Lemasson J. J., de Micco P., de Lamballerie X. 2004; Sequences of flavivirus-related RNA viruses persist in DNA form integrated in the genome of Aedes spp. mosquitoes. J Gen Virol 85:1971–1980 [View Article][PubMed]
    [Google Scholar]
  15. Darriba D., Taboada G. L., Doallo R., Posada D. 2011; ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164–1165 [View Article][PubMed]
    [Google Scholar]
  16. Darriba D., Taboada G. L., Doallo R., Posada D. 2012; jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772 [View Article][PubMed]
    [Google Scholar]
  17. de Lamballerie X., Crochu S., Billoir F., Neyts J., de Micco P., Holmes E. C., Gould E. A. 2002; Genome sequence analysis of Tamana bat virus and its relationship with the genus Flavivirus. J Gen Virol 83:2443–2454[PubMed]
    [Google Scholar]
  18. Delport W., Poon A. F. Y., Frost S. D. W., Kosakovsky Pond S. L. 2010; Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26:2455–2457 [View Article][PubMed]
    [Google Scholar]
  19. Dixon E. J. 2013; Late Pleistocene colonization of North America from Northeast Asia: new insights from large-scale paleogeographic reconstructions. Quartern Int 285:57–67 [View Article]
    [Google Scholar]
  20. Drummond A. J., Pybus O. G., Rambaut A., Forsberg R., Rodrigo A. G. 2003; Measurably evolving populations. Trends Ecol Evol 18:481–488 [View Article]
    [Google Scholar]
  21. Drummond A. J., Rambaut A., Shapiro B., Pybus O. G. 2005; Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192 [View Article][PubMed]
    [Google Scholar]
  22. Drummond A. J., Suchard M. A., Xie D., Rambaut A. 2012; Bayesian phylogenetics with BEAUti and the beast 1.7. Mol Biol Evol 29:1969–1973 [View Article][PubMed]
    [Google Scholar]
  23. Duffy S., Shackelton L. A., Holmes E. C. 2008; Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9:267–276 [View Article][PubMed]
    [Google Scholar]
  24. Dunham E. J., Holmes E. C. 2007; Inferring the timescale of dengue virus evolution under realistic models of DNA substitution. J Mol Evol 64:656–661 [View Article][PubMed]
    [Google Scholar]
  25. Dyke A. S. 2004; An outline of the deglaciation of North America with emphasis on central and northern Canada. In Quaternary Glaciations, Extent and Chronology Part II: North America pp. 373–424 Edited by Ehlers J., Gibbard P. L. Amsterdam: Elsevier; [View Article]
    [Google Scholar]
  26. Ebel G. D. 2010; Update on Powassan virus: emergence of a North American tick-borne flavivirus. Annu Rev Entomol 55:95–110 [View Article][PubMed]
    [Google Scholar]
  27. Ebel G. D., Campbell E. N., Goethert H. K., Spielman A., Telford S. R. III 2000; Enzootic transmission of deer tick virus in New England and Wisconsin sites. Am J Trop Med Hyg 63:36–42[PubMed]
    [Google Scholar]
  28. Elias S. A. 2001; Beringian paleoecology: results from the 1997 workshop. Quatern Sci Rev 20:7–13 [View Article]
    [Google Scholar]
  29. Elias S. A., Short S. K., Nelson C. H., Birks H. H. 1996; Life and times of the Bering land bridge. Nature 382:60–63 [View Article]
    [Google Scholar]
  30. Fagundes N. J. R., Kanitz R., Eckert R., Valls A. C. S., Bogo M. R., Salzano F. M., Smith D. G., Silva W. A. Jr, Zago M. A.other authors 2008; Mitochondrial population genomics supports a single pre-Clovis origin with a coastal route for the peopling of the Americas. Am J Hum Genet 82:583–592 [View Article][PubMed]
    [Google Scholar]
  31. Falush D., Wirth T., Linz B., Pritchard J. K., Stephens M., Kidd M., Blaser M. J., Graham D. Y., Vacher S.other authors 2003; Traces of human migrations in Helicobacter pylori populations. Science 299:1582–1585 [View Article][PubMed]
    [Google Scholar]
  32. Gaunt M. W., Sall A. A., de Lamballerie X., Falconar A. K., Dzhivanian T. I., Gould E. A. 2001; Phylogenetic relationships of flaviviruses correlate with their epidemiology, disease association and biogeography. J Gen Virol 82:1867–1876[PubMed]
    [Google Scholar]
  33. Goebel T., Buvit I.editors 2011 From the Yenisei to the Yukon: Interpreting Lithic Assemblage Variability in Late Pleistocene/Early Holocene Beringia College Station, TX: Texas A&M University Press;
    [Google Scholar]
  34. Goebel T., Waters M. R., O’Rourke D. H. 2008; The late Pleistocene dispersal of modern humans in the Americas. Science 319:1497–1502 [View Article][PubMed]
    [Google Scholar]
  35. Gould E. A., Solomon T. 2008; Pathogenic flaviviruses. Lancet 371:500–509 [View Article][PubMed]
    [Google Scholar]
  36. Gould E. A., de Lamballerie X., Zanotto P. M., Holmes E. C. 2001; Evolution, epidemiology, and dispersal of flaviviruses revealed by molecular phylogenies. Adv Virus Res 57:71–103 [View Article][PubMed]
    [Google Scholar]
  37. Gould E. A., de Lamballerie X., Zanotto P. M., Holmes E. C. 2003; Origins, evolution, and vector/host coadaptations within the genus Flavivirus. Adv Virus Res 59:277–314 [View Article][PubMed]
    [Google Scholar]
  38. Gouy M., Guindon S., Gascuel O. 2010; SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224 [View Article][PubMed]
    [Google Scholar]
  39. Grard G., Moureau G., Charrel R. N., Lemasson J.-J., Gonzalez J.-P., Gallian P., Gritsun T. S., Holmes E. C., Gould E. A., de Lamballerie X. 2007; Genetic characterization of tick-borne flaviviruses: new insights into evolution, pathogenetic determinants and taxonomy. Virology 361:80–92 [View Article][PubMed]
    [Google Scholar]
  40. Grard G., Moureau G., Charrel R. N., Holmes E. C., Gould E. A., de Lamballerie X. 2010; Genomics and evolution of Aedes-borne flaviviruses. J Gen Virol 91:87–94 [View Article][PubMed]
    [Google Scholar]
  41. Gritsun T. S., Nuttall P. A., Gould E. A. 2003; Tick-borne flaviviruses. Adv Virus Res 61:317–371 [View Article][PubMed]
    [Google Scholar]
  42. Gubler D., Kuno G., Markoff L. 2007; Flaviviruses. In Fields Virology, 5th edn. vol. 1 pp. 1153–1253 Edited by Knipe D., Howley P., Griffin D., Lamb R., Martin M., Roizman B., Straus S. Philadelphia, PA: Lippincott-Raven;
    [Google Scholar]
  43. Hanada K., Suzuki Y., Gojobori T. 2004; A large variation in the rates of synonymous substitution for RNA viruses and its relationship to a diversity of viral infection and transmission modes. Mol Biol Evol 21:1074–1080 [View Article][PubMed]
    [Google Scholar]
  44. Heaton T. H., Grady F. 2003; The late Wisconsin vertebrate history of Prince of Wales Island, Southeast Alaska. In Ice Age Cave Faunas of North America pp. 17–53 Edited by Schubert B. W., Mead J. I., Graham R. W. Bloomington, IN: Indiana University Press;
    [Google Scholar]
  45. Heinze D. M., Gould E. A., Forrester N. L. 2012; Revisiting the clinal concept of evolution and dispersal for the tick-borne flaviviruses by using phylogenetic and biogeographic analyses. J Virol 86:8663–8671 [View Article][PubMed]
    [Google Scholar]
  46. Henn B. M., Cavalli-Sforza L. L., Feldman M. W. 2012; The great human expansion. Proc Natl Acad Sci U S A 109:17758–17764 [View Article][PubMed]
    [Google Scholar]
  47. Hey J. 2005; On the number of New World founders: a population genetic portrait of the peopling of the Americas. PLoS Biol 3:e193 [View Article][PubMed]
    [Google Scholar]
  48. Hinten S. R., Beckett G. A., Gensheimer K. F., Pritchard E., Courtney T. M., Sears S. D., Woytowicz J. M., Preston D. G., Smith R. P. Jrother authors 2008; Increased recognition of Powassan encephalitis in the United States, 1999–2005. Vector Borne Zoonotic Dis 8:733–740 [View Article][PubMed]
    [Google Scholar]
  49. Ho S. Y. W., Phillips M. J. 2009; Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Syst Biol 58:367–380 [View Article][PubMed]
    [Google Scholar]
  50. Holmes E. C. 2003a; Molecular clocks and the puzzle of RNA virus origins. J Virol 77:3893–3897 [View Article][PubMed]
    [Google Scholar]
  51. Holmes E. C. 2003b; Patterns of intra- and interhost nonsynonymous variation reveal strong purifying selection in dengue virus. J Virol 77:11296–11298 [View Article][PubMed]
    [Google Scholar]
  52. Holmes E. C. 2004; The phylogeography of human viruses. Mol Ecol 13:745–756 [View Article][PubMed]
    [Google Scholar]
  53. Hoshino K., Isawa H., Tsuda Y., Sawabe K., Kobayashi M. 2009; Isolation and characterization of a new insect flavivirus from Aedes albopictus and Aedes flavopictus mosquitoes in Japan. Virology 391:119–129 [View Article][PubMed]
    [Google Scholar]
  54. Huhtamo E., Putkuri N., Kurkela S., Manni T., Vaheri A., Vapalahti O., Uzcátegui N. Y. 2009; Characterization of a novel flavivirus from mosquitoes in northern europe that is related to mosquito-borne flaviviruses of the tropics. J Virol 83:9532–9540 [View Article][PubMed]
    [Google Scholar]
  55. Hultén E. 1937 Outline of the History of Arctic and Boreal Biota During the Quaternary Period Stockholm: Bokforlagsaktiebolaget Thule;
    [Google Scholar]
  56. Jenkins G. M., Rambaut A., Pybus O. G., Holmes E. C. 2002; Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J Mol Evol 54:156–165 [View Article][PubMed]
    [Google Scholar]
  57. Katoh K., Standley D. M. 2013; mafft multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780 [View Article][PubMed]
    [Google Scholar]
  58. Katzourakis A., Gifford R. J. 2010; Endogenous viral elements in animal genomes. PLoS Genet 6:e1001191 [View Article][PubMed]
    [Google Scholar]
  59. Katzourakis A., Gifford R. J., Tristem M., Gilbert M. T. P., Pybus O. G. 2009; Macroevolution of complex retroviruses. Science 325:1512 [View Article][PubMed]
    [Google Scholar]
  60. Kelly R. L. 2003; Maybe we do know when people first came to North America; and what does it mean if we do?. Quartern Int 109–110:133–145 [View Article]
    [Google Scholar]
  61. Klungthong C., Zhang C., Mammen M. P. Jr, Ubol S., Holmes E. C. 2004; The molecular epidemiology of dengue virus serotype 4 in Bangkok, Thailand. Virology 329:168–179 [View Article][PubMed]
    [Google Scholar]
  62. Kolodziejek J., Pachler K., Bin H., Mendelson E., Shulman L., Orshan L., Nowotny N. 2013; Barkedji virus, a novel mosquito-borne flavivirus identified in Culex perexiguus mosquitoes, Israel, 2011. J Gen Virol 94:2449–2457 [View Article][PubMed]
    [Google Scholar]
  63. Korber B., Muldoon M., Theiler J., Gao F., Gupta R., Lapedes A., Hahn B. H., Wolinsky S., Bhattacharya T. 2000; Timing the ancestor of the HIV-1 pandemic strains. Science 288:1789–1796 [View Article][PubMed]
    [Google Scholar]
  64. Kumar S. R. P., Patil J. A., Cecilia D., Cherian S. S., Barde P. V., Walimbe A. M., Yadav P. D., Yergolkar P. N., Shah P. S.other authors 2010; Evolution, dispersal and replacement of American genotype dengue type 2 viruses in India (1956–2005): selection pressure and molecular clock analyses. J Gen Virol 91:707–720 [View Article][PubMed]
    [Google Scholar]
  65. Kuno G. 2007; Host range specificity of flaviviruses: correlation with in vitro replication. J Med Entomol 44:93–101 [View Article][PubMed]
    [Google Scholar]
  66. Kuno G., Chang G.-J. J. 2006; Characterization of Sepik and Entebbe bat viruses closely related to yellow fever virus. Am J Trop Med Hyg 75:1165–1170[PubMed]
    [Google Scholar]
  67. Lee J. S., Grubaugh N. D., Kondig J. P., Turell M. J., Kim H.-C., Klein T. A., O’Guinn M. L. 2013; Isolation and genomic characterization of Chaoyang virus strain ROK144 from Aedes vexans nipponii from the Republic of Korea. Virology 435:220–224 [View Article][PubMed]
    [Google Scholar]
  68. Lindenbach B. D., Rice C. M. 2003; Molecular biology of flaviviruses. Adv Virus Res 59:23–61 [View Article][PubMed]
    [Google Scholar]
  69. Lindenbach B. D., Thiel H.-J., Rice C. M. 2007; Flaviviridae: the viruses and their replication. In Fields Virology, 5th edn. vol. 1 pp. 1101–1152 Edited by Knipe D., Howley P., Griffin D., Lamb R., Martin M., Roizman B., Straus S. Philadelphia, PA: Lippincott-Raven;
    [Google Scholar]
  70. Linz B., Balloux F., Moodley Y., Manica A., Liu H., Roumagnac P., Falush D., Stamer C., Prugnolle F.other authors 2007; An African origin for the intimate association between humans and Helicobacter pylori. Nature 445:915–918 [View Article][PubMed]
    [Google Scholar]
  71. Lobo F. P., Mota B. E. F., Pena S. D. J., Azevedo V., Macedo A. M., Tauch A., Machado C. R., Franco G. R. 2009; Virus–host coevolution: common patterns of nucleotide motif usage in Flaviviridae and their hosts. PLoS ONE 4:e6282 [View Article][PubMed]
    [Google Scholar]
  72. Lutomiah J. J. L., Mwandawiro C., Magambo J., Sang R. C. 2007; Infection and vertical transmission of Kamiti river virus in laboratory bred Aedes aegypti mosquitoes. J Insect Sci 7:1–7 [View Article][PubMed]
    [Google Scholar]
  73. Macaulay V., Hill C., Achilli A., Rengo C., Clarke D., Meehan W., Blackburn J., Semino O., Scozzari R.other authors 2005; Single, rapid coastal settlement of Asia revealed by analysis of complete mitochondrial genomes. Science 308:1034–1036 [View Article][PubMed]
    [Google Scholar]
  74. Mackenzie J. S., Gubler D. J., Petersen L. R. 2004; Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat Med 10:SupplS98–S109 [View Article][PubMed]
    [Google Scholar]
  75. Mandryk C. A., Josenhans H., Fedje D. W., Mathewes R. W. 2001; Late Quaternary paleoenvironments of Northwestern North America: implications for inland versus coastal migration routes. Quat Sci Rev 20:301–314 [View Article]
    [Google Scholar]
  76. May F. J., Davis C. T., Tesh R. B., Barrett A. D. T. 2011; Phylogeography of West Nile virus: from the cradle of evolution in Africa to Eurasia, Australia, and the Americas. J Virol 85:2964–2974 [View Article][PubMed]
    [Google Scholar]
  77. McDougall I., Brown F. H., Fleagle J. G. 2005; Stratigraphic placement and age of modern humans from Kibish, Ethiopia. Nature 433:733–736 [View Article][PubMed]
    [Google Scholar]
  78. Medeiros D. B. A., Nunes M. R. T., Vasconcelos P. F. C., Chang G.-J. J., Kuno G. 2007; Complete genome characterization of Rocio virus (Flavivirus: Flaviviridae), a Brazilian flavivirus isolated from a fatal case of encephalitis during an epidemic in Sao Paulo state. J Gen Virol 88:2237–2246 [View Article][PubMed]
    [Google Scholar]
  79. Mehla R., Kumar S. R. P., Yadav P., Barde P. V., Yergolkar P. N., Erickson B. R., Carroll S. A., Mishra A. C., Nichol S. T., Mourya D. T. 2009; Recent ancestry of Kyasanur Forest disease virus. Emerg Infect Dis 15:1431–1437 [View Article][PubMed]
    [Google Scholar]
  80. Miller M. A., Pfeiffer W., Schwartz T. 2010; Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Presented at the Gateway Computing Environments Workshop, 2010
    [Google Scholar]
  81. Mohammed M. A. F., Galbraith S. E., Radford A. D., Dove W., Takasaki T., Kurane I., Solomon T. 2011; Molecular phylogenetic and evolutionary analyses of Muar strain of Japanese encephalitis virus reveal it is the missing fifth genotype. Infect Genet Evol 11:855–862 [View Article][PubMed]
    [Google Scholar]
  82. Moodley Y., Linz B., Bond R. P., Nieuwoudt M., Soodyall H., Schlebusch C. M., Bernhöft S., Hale J., Suerbaum S.other authors 2012; Age of the association between Helicobacter pylori and man. PLoS Pathog 8:e1002693 [View Article][PubMed]
    [Google Scholar]
  83. Pan X.-L., Liu H., Wang H.-Y., Fu S.-H., Liu H.-Z., Zhang H.-L., Li M.-H., Gao X.-Y., Wang J.-L.other authors 2011; Emergence of genotype I of Japanese encephalitis virus as the dominant genotype in Asia. J Virol 85:9847–9853 [View Article][PubMed]
    [Google Scholar]
  84. Patil J. A., Cherian S., Walimbe A. M., Patil B. R., Sathe P. S., Shah P. S., Cecilia D. 2011; Evolutionary dynamics of the American African genotype of dengue type 1 virus in India (1962–2005). Infect Genet Evol 11:1443–1448 [View Article][PubMed]
    [Google Scholar]
  85. Pond S. L. K., Frost S. D. W., Muse S. V. 2005; HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679 [View Article][PubMed]
    [Google Scholar]
  86. Porterfield J. S. 1980; Antigenic characteristics and classification of Togaviridae. In The Togaviruses: Biology, Structure, Replication pp. 13–46 Edited by Schlesinger R. W. New York: Academic Press; [View Article]
    [Google Scholar]
  87. Pybus O. G., Rambaut A., Belshaw R., Freckleton R. P., Drummond A. J., Holmes E. C. 2007; Phylogenetic evidence for deleterious mutation load in RNA viruses and its contribution to viral evolution. Mol Biol Evol 24:845–852 [View Article][PubMed]
    [Google Scholar]
  88. Ramírez A., Fajardo A., Moros Z., Gerder M., Caraballo G., Camacho D., Comach G., Alarcón V., Zambrano J.other authors 2010; Evolution of dengue virus type 3 genotype III in Venezuela: diversification, rates and population dynamics. Virol J 7:329 [View Article][PubMed]
    [Google Scholar]
  89. Rasmussen M., Guo X., Wang Y., Lohmueller K. E., Rasmussen S., Albrechtsen A., Skotte L., Lindgreen S., Metspalu M.other authors 2011; An Aboriginal Australian genome reveals separate human dispersals into Asia. Science 334:94–98 [View Article][PubMed]
    [Google Scholar]
  90. Ronquist F., Teslenko M., van der Mark P., Ayres D. L., Darling A., Höhna S., Larget B., Liu L., Suchard M. A., Huelsenbeck J. P. 2012; MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542 [View Article][PubMed]
    [Google Scholar]
  91. Sanjuán R. 2012; From molecular genetics to phylodynamics: evolutionary relevance of mutation rates across viruses. PLoS Pathog 8:e1002685 [View Article][PubMed]
    [Google Scholar]
  92. Schurr T. G. 2004; The peopling of the new world: perspectives from molecular anthropology. Annu Rev Anthropol 33:551–583 [View Article]
    [Google Scholar]
  93. Shapiro B., Drummond A. J., Rambaut A., Wilson M. C., Matheus P. E., Sher A. V., Pybus O. G., Gilbert M. T. P., Barnes I.other authors 2004; Rise and fall of the Beringian steppe bison. Science 306:1561–1565 [View Article][PubMed]
    [Google Scholar]
  94. Shapiro B., Rambaut A., Drummond A. J. 2006; Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 23:7–9 [View Article][PubMed]
    [Google Scholar]
  95. Sharp P. M., Simmonds P. 2011; Evaluating the evidence for virus/host co-evolution. Curr Opin Virol 1:436–441 [View Article][PubMed]
    [Google Scholar]
  96. Stamatakis A. 2006; RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690 [View Article][PubMed]
    [Google Scholar]
  97. Stringer C. B., Andrews P. 1988; Genetic and fossil evidence for the origin of modern humans. Science 239:1263–1268 [View Article][PubMed]
    [Google Scholar]
  98. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
    [Google Scholar]
  99. Twiddy S. S., Holmes E. C., Rambaut A. 2003; Inferring the rate and time-scale of dengue virus evolution. Mol Biol Evol 20:122–129 [View Article][PubMed]
    [Google Scholar]
  100. Uzcátegui N. Y., Sironen T., Golovljova I., Jääskeläinen A. E., Välimaa H., Lundkvist A., Plyusnin A., Vaheri A., Vapalahti O. 2012; Rate of evolution and molecular epidemiology of tick-borne encephalitis virus in Europe, including two isolations from the same focus 44 years apart. J Gen Virol 93:786–796 [View Article][PubMed]
    [Google Scholar]
  101. Wasik B. R., Turner P. E. 2013; On the biological success of viruses. Annu Rev Microbiol 67:519–541 [View Article][PubMed]
    [Google Scholar]
  102. Weidmann M., Frey S., Freire C. C. M., Essbauer S., Růžek D., Klempa B., Zubrikova D., Vögerl M., Pfeffer M.other authors 2013; Molecular phylogeography of tick-borne encephalitis virus in central Europe. J Gen Virol 94:2129–2139 [View Article][PubMed]
    [Google Scholar]
  103. Wertheim J. O., Kosakovsky Pond S. L. 2011; Purifying selection can obscure the ancient age of viral lineages. Mol Biol Evol 28:3355–3365 [View Article][PubMed]
    [Google Scholar]
  104. Wirth T., Hildebrand F., Allix-Béguec C., Wölbeling F., Kubica T., Kremer K., van Soolingen D., Rüsch-Gerdes S., Locht C.other authors 2008; Origin, spread and demography of the Mycobacterium tuberculosis complex. PLoS Pathog 4:e1000160 [View Article][PubMed]
    [Google Scholar]
  105. Woelk C. H., Holmes E. C. 2002; Reduced positive selection in vector-borne RNA viruses. Mol Biol Evol 19:2333–2336 [View Article][PubMed]
    [Google Scholar]
  106. Worobey M., Telfer P., Souquière S., Hunter M., Coleman C. A., Metzger M. J., Reed P., Makuwa M., Hearn G.other authors 2010; Island biogeography reveals the deep history of SIV. Science 329:1487 [View Article][PubMed]
    [Google Scholar]
  107. Yang Z. 1996; Maximum-likelihood models for combined analyses of multiple sequence data. J Mol Evol 42:587–596 [View Article][PubMed]
    [Google Scholar]
  108. Zanotto P. M., Gao G. F., Gritsun T., Marin M. S., Jiang W. R., Venugopal K., Reid H. W., Gould E. A. 1995; An arbovirus cline across the northern hemisphere. Virology 210:152–159 [View Article][PubMed]
    [Google Scholar]
  109. Zanotto P. M., Gould E. A., Gao G. F., Harvey P. H., Holmes E. C. 1996; Population dynamics of flaviviruses revealed by molecular phylogenies. Proc Natl Acad Sci U S A 93:548–553 [View Article][PubMed]
    [Google Scholar]
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