European and Asian viruses within the tick-borne encephalitis flavivirus complex are known to show temporal, spatial and phylogenetic relationships that imply a clinal pattern of evolution. However, the isolation of recognized Far-Eastern tick-borne encephalitis virus (TBEV) strains in the European region of the former Soviet Union (SU), i.e. thousands of kilometres west of the region in which they are considered endemic, appears to contradict this concept. Here, we present a parsimonious explanation for this apparent anomaly based on analysis of the dates and regions in which these non-endemic strains were isolated, together with their phylogenetic relationships and the records of redistribution of animals under the All-Union programme for acclimatization of game animals within the former SU. Our evidence supports the concept that the anomalous distribution of Far-Eastern TBEV strains in Europe and Siberia arose primarily as the result of the large-scale westward redistribution of game animals for economic purposes.


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  1. Ando, K., Kuratsuka, K., Arima, S., Hironaka, N., Honda, Y. & Ishii, K.(1952). Studies on the viruses isolated during epidemic of Japanese B encephalitis in 1948 in Tokyo area. Kitasato Arch Exp Med 24, 557–562 (in Japanese ). [Google Scholar]
  2. Bakhvalova, V. N., Dobrotvorsky, A. K., Panov, V. V., Matveeva, V. A., Tkachev, S. E. & Morozova, O. V.(2006). Natural tick-borne encephalitis virus infection among wild small mammals in the southeastern part of Western Siberia, Russia. Vector Borne Zoonotic Dis 6, 32–41.[CrossRef] [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.[CrossRef] [Google Scholar]
  4. Ecker, M., Allison, S. L., Meixner, T. & Heinz, F. X.(1999). Sequence analysis and genetic classification of tick-borne encephalitis viruses from Europe and Asia. J Gen Virol 80, 179–185. [Google Scholar]
  5. Filippova, N. A. (editor)(1985).Taiga tick Ixodes persulcatus Schulze (Acarina, Ixodidae). Morphology, Systematics, Ecology, Medical Importance. Leningrad, USSR. : Nauka (in Russian). [Google Scholar]
  6. Haglund, M., Vene, S., Forsgren, M., Gunther, G., Johansson, B., Niedrig, M., Plyusnin, A., Lindquist, L. & Lundkvist, A.(2003). Characterisation of human tick-borne encephalitis virus from Sweden. J Med Virol 71, 610–621.[CrossRef] [Google Scholar]
  7. 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. [Google Scholar]
  8. Hoogstraal, H., Kaiser, M. N., Traylor, M. A., Guindy, E. & Gaber, S.(1963). Ticks (Ixodidae) on birds migrating from Europe and Asia to Africa 1959–61. Bull World Health Organ 28, 235–262. [Google Scholar]
  9. 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.[CrossRef] [Google Scholar]
  10. 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, 7–13.[CrossRef] [Google Scholar]
  11. 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.[CrossRef] [Google Scholar]
  12. 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.[CrossRef] [Google Scholar]
  13. Labuda, M., Jones, L. D., Williams, T., Danielova, V. & Nuttall, P. A.(1993). Efficient transmission of tick-borne encephalitis virus between cofeeding ticks. J Med Entomol 30, 295–299.[CrossRef] [Google Scholar]
  14. 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.[CrossRef] [Google Scholar]
  15. 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. [Google Scholar]
  16. Mickiené, A., Vene, S., Golovljova, I., Laiškonis, A., Lindquist, L., Plyusnin, A. & Lundkvist, Å.(2001). Tick-borne encephalitis virus in Lithuania. Eur J Clin Microbiol Infect Dis 20, 886–888.[CrossRef] [Google Scholar]
  17. Pavlov, M. P.(1996).Acclimatization of Game Mammals and Birds in the USSR, Part 4. Kirov, Russia. : Russian Academy of Agricultural Sciences (in Russian ). [Google Scholar]
  18. Pavlov, M. P.(1999).Acclimatization of Game Mammals and Birds in the USSR, Part 3. Kirov, Russia. : Russian Academy of Agricultural Sciences (in Russian ). [Google Scholar]
  19. Pavlov, M. P., Korsakova, I. B., Timofeev, E. V. & Safonov, V. G.(1973).Acclimatization of Game Mammals and Birds in the USSR, Part 1. Kirov, USSR. : Volgo-Vyatskoe. [Google Scholar]
  20. Pavlov, M. P., Korsakova, I. B. & Lavrov, N. P.(1974).Acclimatization of Game Mammals and Birds in the USSR, Part 2. Kirov, USSR. : Volgo-Vyatskoe. [Google Scholar]
  21. Pavlovsky, E. N.(1947). Ticks and tick-borne encephalitis. In Parasitology of the Far East, pp. 212–264. Edited by Pavlovsky, E. N.. Leningrad. : Medgiz (in Russian). [Google Scholar]
  22. Pogodina, V. V., Karan, L. S., Koliasnikova, N. M., Levina, L. S., Malenko, G. V., Gamova, E. G., Lesnikova, M. V., Kiliachina, A. S., Esiunina, M. S. & other authors(2007). Evolution of tick-borne encephalitis and a problem of evolution of its causative agent. Vopr Virusol 52, 16–21 (in Russian). [Google Scholar]
  23. Suzuki, Y.(2007). Multiple transmissions of tick-borne encephalitis virus between Japan and Russia. Genes Genet Syst 82, 187–195.[CrossRef] [Google Scholar]
  24. Venugopal, K., Buckley, A., Reid, H. W. & Gould, E. A.(1992). Nucleotide sequence of the envelope glycoprotein of Negishi virus shows very close homology to louping ill virus. Virology 190, 515–521.[CrossRef] [Google Scholar]
  25. 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.[CrossRef] [Google Scholar]
  26. Yun, S. M., Kim, S. Y., Han, M. G., Jeong, Y. E., Yong, T. S., Lee, C. H. & Ju, Y. R.(2009). Analysis of the envelope (E) protein gene of tick-borne encephalitis viruses isolated in South Korea. Vector Borne Zoonotic Dis 9, 287–293.[CrossRef] [Google Scholar]
  27. 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.[CrossRef] [Google Scholar]
  28. Zlobin, V. I., Demina, T. V., Belikov, S. I., Butina, T. V., Gorin, O. Z., Adel'shin, R. V. & Grachev, M. A.(2001a). Genetic typing of tick-borne encephalitis virus based on an analysis of the levels of homology of a membrane protein gene fragment. Vopr Virusol 46, 17–22 (in Russian). [Google Scholar]
  29. Zlobin, V. I., Demina, T. V., Mamaev, L. V., Butina, T. V., Belikov, S. I., Gorin, O. Z., Dzhioev Iu, P., Verkhozina, M. M., Kozlova, I. V. & other authors(2001b). Analysis of genetic variability of strains of tick-borne encephalitis virus by primary structure of a fragment of the membrane protein E gene. Vopr Virusol 46, 12–16 (in Russian). [Google Scholar]

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vol. , part 12, pp. 2941–2946

Tick-borne encephalitis virus (TBEV) strains of the Far-Eastern subtype that were compared by phylogenetic analysis.

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