1887

Abstract

Tick-borne encephalitis virus (TBEV) is a member of the family . It is transmitted by spp. ticks in a cycle involving rodents and small mammals. TBEV has three subtypes: European, Siberian and Far Eastern. The virus causes thousands of cases of meningoencephalitis in Europe annually, with an increasing trend. The increase may be attributed to a complex network of elements, including climatic, environmental and socio-economic factors. In an attempt to understand the evolutionary history and dispersal of TBEV, to existing genetic data we add two novel complete ORF sequences of TBEV strains from northern Europe and the completion of the genome of four others. Moreover, we provide a unique measure for the natural rate of evolution of TBEV by studying two isolations from the same forest on an island in Åland archipelago 44 years apart. For all isolates, we analysed the phylogeny, rate of evolution and probable time of radiation of the different TBEV strains. The results show that the two lineages of TBEV in different species have evolved independently for approximately 3300 years. Notably, rapid radiation of TBEV-Eur occurred approximately 300 years ago, without the large-scale geographical clustering observed previously for the Siberian subtype. The measurements from the natural rate of evolution correlated with the estimates done by phylogenetic programs, demonstrating their robustness.

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2012-04-01
2024-03-29
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References

  1. Anderson J. F., Magnarelli L. A. 2008; Biology of ticks. Infect Dis Clin North Am 22:195–215 [View Article][PubMed]
    [Google Scholar]
  2. Asikainen K., Hänninen T., Henttonen H., Niemimaa J., Laakkonen J., Andersen H. K., Bille N., Leirs H., Vaheri A., Plyusnin A. 2000; Molecular evolution of Puumala hantavirus in Fennoscandia: phylogenetic analysis of strains from two recolonization routes, Karelia and Denmark. J Gen Virol 81:2833–2841[PubMed]
    [Google Scholar]
  3. Bakhvalova V. N., Potapova O. F., Panov V. V., Morozova O. V. 2009; Vertical transmission of tick-borne encephalitis virus between generations of adapted reservoir small rodents. Virus Res 140:172–178 [View Article][PubMed]
    [Google Scholar]
  4. Bourhy H., Kissi B., Audry L., Smreczak M., Sadkowska-Todys M., Kulonen K., Tordo N., Zmudzinski J. F., Holmes E. C. 1999; Ecology and evolution of rabies virus in Europe. J Gen Virol 80:2545–2557[PubMed]
    [Google Scholar]
  5. Brummer-Korvenkontio M., Saikku P., Korhonen P., Oker-Blom N. 1973; Arboviruses in Finland. I. Isolation of tick-borne encephalitis (TBE) virus from arthropods, vertebrates, and patients. Am J Trop Med Hyg 22:382–389[PubMed]
    [Google Scholar]
  6. Charrel R. N., Attoui H., Butenko A. M., Clegg J. C., Deubel V., Frolova T. V., Gould E. A., Gritsun T. S., Heinz F. X. other authors 2004; Tick-borne virus diseases of human interest in Europe. Clin Microbiol Infect 10:1040–1055 [View Article][PubMed]
    [Google Scholar]
  7. 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]
  8. Danielová V., Holubová J. 1991; Transovarial transmission rate of tick-borne encephalitis virus in Ixodes ricinus ticks. In Modern Acarology pp. 7–10 Edited by Dusbabek F., Bukva V. The Hague: Academia, Prague and SPB Academic Publishing;
    [Google Scholar]
  9. Danielová V., Kliegrová S., Daniel M., Benes C. 2008; Influence of climate warming on tickborne encephalitis expansion to higher altitudes over the last decade (1997–2006) in the Highland Region (Czech Republic). Cent Eur J Public Health 16:4–11[PubMed]
    [Google Scholar]
  10. Drummond A. J., Rambaut A. 2007; beast: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214 [View Article][PubMed]
    [Google Scholar]
  11. Edgar R. C. 2004; muscle: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113 [View Article][PubMed]
    [Google Scholar]
  12. Estrada-Peña A., Jongejan F. 1999; Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp Appl Acarol 23:685–715 [View Article][PubMed]
    [Google Scholar]
  13. Felsenstein J. 1989; phylip – phylogeny inference package (version 3.2). Cladistics 5:164–166
    [Google Scholar]
  14. 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]
  15. Golovljova I., Vene S., Sjölander K. B., Vasilenko V., Plyusnin A., Lundkvist Å. 2004; Characterization of tick-borne encephalitis virus from Estonia. J Med Virol 74:580–588 [View Article][PubMed]
    [Google Scholar]
  16. Golovljova I., Katargina O., Geller J., Tallo T., Mittzenkov V., Vene S., Nemirov K., Kutsenko A., Kilosanidze G. other authors 2008; Unique signature amino acid substitution in Baltic tick-borne encephalitis virus (TBEV) strains within the Siberian TBEV subtype. Int J Med Microbiol 298:Suppl. 1108–120 [View Article]
    [Google Scholar]
  17. 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]
  18. 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]
  19. Gritsun T. S., Frolova T. V., Zhankov A. I., Armesto M., Turner S. L., Frolova M. P., Pogodina V. V., Lashkevich V. A., Gould E. A. 2003; Characterization of a siberian virus isolated from a patient with progressive chronic tick-borne encephalitis. J Virol 77:25–36 [View Article][PubMed]
    [Google Scholar]
  20. Haglund M., Forsgren M., Lindh G., Lindquist L. 1996; A 10-year follow-up study of tick-borne encephalitis in the Stockholm area and a review of the literature: need for a vaccination strategy. Scand J Infect Dis 28:217–224 [View Article][PubMed]
    [Google Scholar]
  21. Han X., Aho M., Vene S., Peltomaa M., Vaheri A., Vapalahti O. 2001; Prevalence of tick-borne encephalitis virus in Ixodes ricinus ticks in Finland. J Med Virol 64:21–28 [View Article][PubMed]
    [Google Scholar]
  22. Hasegawa M., Kishino H., Yano T. 1985; Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174 [View Article][PubMed]
    [Google Scholar]
  23. Hasle G., Bjune G., Edvardsen E., Jakobsen C., Linnehol B., Røer J. E., Mehl R., Røed K. H., Pedersen J., Leinaas H. P. 2009; Transport of ticks by migratory passerine birds to Norway. J Parasitol 95:1342–1351 [View Article][PubMed]
    [Google Scholar]
  24. Hayasaka D., Suzuki Y., Kariwa H., Ivanov L., Volkov V., Demenev V., Mizutani T., Gojobori T., Takashima I. 1999; Phylogenetic and virulence analysis of tick-borne encephalitis viruses from Japan and far-Eastern Russia. J Gen Virol 80:3127–3135[PubMed]
    [Google Scholar]
  25. Heinz F. X., Holzmann H., Essl A., Kundi M. 2007; Field effectiveness of vaccination against tick-borne encephalitis. Vaccine 25:7559–7567 [View Article][PubMed]
    [Google Scholar]
  26. Holzmann H., Aberle S. W., Stiasny K., Werner P., Mischak A., Zainer B., Netzer M., Koppi S., Bechter E., Heinz F. X. 2009; Tick-borne encephalitis from eating goat cheese in a mountain region of Austria. Emerg Infect Dis 15:1671–1673[PubMed] [CrossRef]
    [Google Scholar]
  27. Jääskeläinen A. E., Tikkakoski T., Uzcátegui N. Y., Alekseev A. N., Vaheri A., Vapalahti O. 2006; Siberian subtype tickborne encephalitis virus, Finland. Emerg Infect Dis 12:1568–1571 [View Article][PubMed]
    [Google Scholar]
  28. Jääskeläinen A. E., Sironen T., Murueva G. B., Subbotina N., Alekseev A. N., Castrén J., Alitalo I., Vaheri A., Vapalahti O. 2010; Tick-borne encephalitis virus in ticks in Finland, Russian Karelia and Buryatia. J Gen Virol 91:2706–2712 [View Article][PubMed]
    [Google Scholar]
  29. Jääskeläinen A. E., Tonteri E., Sironen T., Pakarinen L., Vaheri A., Vapalahti O. 2011; European subtype tick-borne encephalitis virus in Ixodes persulcatus ticks. Emerg Infect Dis 17:323–325[PubMed] [CrossRef]
    [Google Scholar]
  30. Juceviciene A., Vapalahti O., Laiskonis A., Ceplikiene J., Leinikki P. 2002; Prevalence of tick-borne-encephalitis virus antibodies in Lithuania. J Clin Virol 25:23–27 [View Article][PubMed]
    [Google Scholar]
  31. Kerbo N., Donchenko I., Kutsar K., Vasilenko V. 2005; Tickborne encephalitis outbreak in Estonia linked to raw goat milk, May–June 2005. Euro Surveill 10:E050623.2[PubMed]
    [Google Scholar]
  32. Kim S. Y., Yun S. M., Han M. G., Lee I. Y., Lee N. Y., Jeong Y. E., Lee B. C., Ju Y. R. 2008; Isolation of tick-borne encephalitis viruses from wild rodents, South Korea. Vector Borne Zoonotic Dis 8:7–14 [View Article][PubMed]
    [Google Scholar]
  33. Kim S. Y., Jeong Y. E., Yun S. M., Lee I. Y., Han M. G., Ju Y. R. 2009; Molecular evidence for tick-borne encephalitis virus in ticks in South Korea. Med Vet Entomol 23:15–20 [View Article][PubMed]
    [Google Scholar]
  34. Kovalev S. Y., Chernykh D. N., Kokorev V. S., Snitkovskaya T. E., Romanenko V. V. 2009; Origin and distribution of tick-borne encephalitis virus strains of the Siberian subtype in the Middle Urals, the north-west of Russia and the Baltic countries. J Gen Virol 90:2884–2892 [View Article][PubMed]
    [Google Scholar]
  35. Kovalev S. Y., Kokorev V. S., Belyaeva I. V. 2010; Distribution of Far-Eastern tick-borne encephalitis virus subtype strains in the former Soviet Union. J Gen Virol 91:2941–2946 [View Article][PubMed]
    [Google Scholar]
  36. Labuda M., Nuttall P. A., Kozuch O., Elecková E., Williams T., Zuffová E., Sabó A. 1993; Non-viraemic transmission of tick-borne encephalitis virus: a mechanism for arbovirus survival in nature. Experientia 49:802–805 [View Article][PubMed]
    [Google Scholar]
  37. Labuda M., Kozuch O., Zuffová E., Elecková E., Hails R. S., Nuttall P. A. 1997; Tick-borne encephalitis virus transmission between ticks cofeeding on specific immune natural rodent hosts. Virology 235:138–143 [View Article][PubMed]
    [Google Scholar]
  38. Lindquist L., Vapalahti O. 2008; Tick-borne encephalitis. Lancet 371:1861–1871 [View Article][PubMed]
    [Google Scholar]
  39. Lindström A., Jaenson T. G. 2003; Distribution of the common tick, Ixodes ricinus (Acari: Ixodidae), in different vegetation types in southern Sweden. J Med Entomol 40:375–378 [View Article][PubMed]
    [Google Scholar]
  40. Lukan M., Bullova E., Petko B. 2010; Climate warming and tick-borne encephalitis, Slovakia. Emerg Infect Dis 16:524–526 [View Article][PubMed]
    [Google Scholar]
  41. Lundkvist Å., Vene S., Golovljova I., Mavtchoutko V., Forsgren M., Kalnina V., Plyusnin A. 2001; Characterization of tick-borne encephalitis virus from Latvia: evidence for co-circulation of three distinct subtypes. J Med Virol 65:730–735 [View Article][PubMed]
    [Google Scholar]
  42. Luterbacher J., Dietrich D., Xoplaki E., Grosjean M., Wanner H. 2004; European seasonal and annual temperature variability, trends, and extremes since 1500. Science 303:1499–1503 [View Article][PubMed]
    [Google Scholar]
  43. Mansfield K. L., Johnson N., Phipps L. P., Stephenson J. R., Fooks A. R., Solomon T. 2009; Tick-borne encephalitis virus – a review of an emerging zoonosis. J Gen Virol 90:1781–1794 [View Article][PubMed]
    [Google Scholar]
  44. Martin D., Rybicki E. 2000; rdp: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563 [View Article][PubMed]
    [Google Scholar]
  45. Mavtchoutko V., Vene S., Haglund M., Forsgren M., Duks A., Kalnina V., Hörling J., Lundkvist A. 2000; Characterization of tick-borne encephalitis virus from Latvia. J Med Virol 60:216–222 [View Article][PubMed]
    [Google Scholar]
  46. McGuire K., Holmes E. C., Gao G. F., Reid H. W., Gould E. A. 1998; Tracing the origins of louping ill virus by molecular phylogenetic analysis. J Gen Virol 79:981–988[PubMed]
    [Google Scholar]
  47. Myat Thu H., Lowry K., Jiang L., Hlaing T., Holmes E. C., Aaskov J. 2005; Lineage extinction and replacement in dengue type 1 virus populations are due to stochastic events rather than to natural selection. Virology 336:163–172 [View Article][PubMed]
    [Google Scholar]
  48. Posada D., Crandall K. A. 1998; modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818 [View Article][PubMed]
    [Google Scholar]
  49. Randolph S. E. 2000; Ticks and tick-borne disease systems in space and from space. Adv Parasitol 47:217–243 [View Article][PubMed]
    [Google Scholar]
  50. Randolph S. E. 2010; To what extent has climate change contributed to the recent epidemiology of tick-borne diseases?. Vet Parasitol 167:92–94 [View Article][PubMed]
    [Google Scholar]
  51. Randolph S. E., Rogers D. J. 2000; Fragile transmission cycles of tick-borne encephalitis virus may be disrupted by predicted climate change. Proc Biol Sci 267:1741–1744 [View Article][PubMed]
    [Google Scholar]
  52. Randolph S. E., Miklisová D., Lysy J., Rogers D. J., Labuda M. 1999; Incidence from coincidence: patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology 118:177–186 [View Article][PubMed]
    [Google Scholar]
  53. Schmidt H. A., Strimmer K., Vingron M., von Haeseler A. 2002; tree-puzzle: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504 [View Article][PubMed]
    [Google Scholar]
  54. 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]
  55. Silber L. A., Soloviev V. D. 1946; Far Eastern tick-borne spring–summer (spring) encephalitis. Am Rev Sov MedSpec. Suppl.1–80[PubMed]
    [Google Scholar]
  56. Sumilo D., Bormane A., Asokliene L., Lucenko I., Vasilenko V., Randolph S. 2006; Tick-borne encephalitis in the Baltic States: identifying risk factors in space and time. Int J Med Microbiol 296:Suppl. 4076–79 [View Article][PubMed]
    [Google Scholar]
  57. Sumilo D., Asokliene L., Bormane A., Vasilenko V., Golovljova I., Randolph S. E. 2007; Climate change cannot explain the upsurge of tick-borne encephalitis in the Baltics. PLoS One 2:e500 [View Article][PubMed]
    [Google Scholar]
  58. Sumilo D., Bormane A., Asokliene L., Vasilenko V., Golovljova I., Avsic-Zupanc T., Hubalek Z., Randolph S. E. 2008a; Socio-economic factors in the differential upsurge of tick-borne encephalitis in Central and Eastern Europe. Rev Med Virol 18:81–95 [View Article][PubMed]
    [Google Scholar]
  59. Sumilo D., Asokliene L., Avsic-Zupanc T., Bormane A., Vasilenko V., Lucenko I., Golovljova I., Randolph S. E. 2008b; Behavioural responses to perceived risk of tick-borne encephalitis: vaccination and avoidance in the Baltics and Slovenia. Vaccine 26:2580–2588 [View Article][PubMed]
    [Google Scholar]
  60. Süss J. 2008; Tick-borne encephalitis in Europe and beyond – the epidemiological situation as of 2007. Euro Surveill 13:18916[PubMed]
    [Google Scholar]
  61. Suzuki Y. 2007; Multiple transmissions of tick-borne encephalitis virus between Japan and Russia. Genes Genet Syst 82:187–195 [View Article][PubMed]
    [Google Scholar]
  62. Tamura K., Dudley J., Nei M., Kumar S. 2007; mega4: molecular evolutionary genetics analysis (mega) software version 4.0. Mol Biol Evol 24:1596–1599 [View Article][PubMed]
    [Google Scholar]
  63. Thiel H. J., Collett M. S., Gould E. A., Heinz F. X., Houghton M., Meyers G., Purcell R. H., Rice C. M. 2005; Family Flaviviridae . In Virus Taxonomy: Classification and Nomenclature. Eighth Report of the International Committee on the Taxonomy of Viruses pp. 981–998 Edited by Fauquet C. M., Mayo M. A., Maniloff J., Desselberger U., Ball L. A. San Diego, CA: Elsevier Academic Press;
    [Google Scholar]
  64. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [View Article][PubMed]
    [Google Scholar]
  65. Tonteri E., Jääskeläinen A. E., Tikkakoski T., Voutilainen L., Niemimaa J., Henttonen H., Vaheri A., Vapalahti O. 2011; Tick-borne encephalitis virus in wild rodents in winter, Finland, 2008–2009. Emerg Infect Dis 17:72–75 [View Article][PubMed]
    [Google Scholar]
  66. Twiddy S. S., Holmes E. C. 2003; The extent of homologous recombination in members of the genus Flavivirus . J Gen Virol 84:429–440 [View Article][PubMed]
    [Google Scholar]
  67. Waldenström J., Lundkvist Å., Falk K. I., Garpmo U., Bergström S., Lindegren G., Sjöstedt A., Mejlon H., Fransson T. other authors 2007; Migrating birds and tickborne encephalitis virus. Emerg Infect Dis 13:1215–1218[PubMed] [CrossRef]
    [Google Scholar]
  68. Whitby J. E., Jennings A. D., Barrett A. D. 1993; Nucleotide sequence of the envelope protein gene of the tick-borne flavivirus, Kumlinge A52. Virus Genes 7:145–149 [View Article][PubMed]
    [Google Scholar]
  69. Xia X., Xie Z. 2001; dambe: software package for data analysis in molecular biology and evolution. J Hered 92:371–373 [View Article][PubMed]
    [Google Scholar]
  70. 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]
  71. 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]
  72. Zeman P., Bene C. 2004; A tick-borne encephalitis ceiling in Central Europe has moved upwards during the last 30 years: possible impact of global warming?. Int J Med Microbiol 293:Suppl. 3748–54[PubMed]
    [Google Scholar]
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