Skip to main content
Springer Nature - PMC COVID-19 Collection logoLink to Springer Nature - PMC COVID-19 Collection
. 2006;299:285–314. doi: 10.1007/3-540-26397-7_10

Evolutionary Influences in Arboviral Disease

S C Weaver 2
Editor: Esteban Domingo1
PMCID: PMC7120121  PMID: 16568903

Abstract

Arthropod-borne viruses (arboviruses) generally require horizontal transmission by arthropod vectors among vertebrate hosts for their natural maintenance. This requirement for alternate replication in disparate hosts places unusual evolutionary constraints on these viruses, which have probably limited the evolution of arboviruses to only a few families of RNA viruses (Togaviridae, Flaviviridae, Bunyaviridae, Rhabdoviridae, Reoviridae, and Orthomyxoviridae) and a single DNA virus. Phylogenetic studies have suggested the dominance of purifying selection in the evolution of arboviruses, consistent with constraints imposed by differing replication environments and requirements in arthropod and vertebrate hosts. Molecular genetic studies of alphaviruses and flaviviruses have also identified several mutations that effect differentially the replication in vertebrate and mosquito cells, consistent with the view that arboviruses must adopt compromise fitness characteristics for each host. More recently, evidence of positive selection has also been obtained from these studies. However, experimental model systems employing arthropod and vertebrate cell cultures have yielded conflicting conclusions on the effect of alternating host infections, with host specialization inconsistently resulting in fitness gains or losses in the bypassed host cells. Further studies using in vivo systems to study experimental arbovirus evolution are critical to understanding and predicting disease emergence, which often results from virus adaptation to new vectors or amplification hosts. Reverse genetic technologies that are now available for most arbovirus groups should be exploited to test assumptions and hypotheses derived from retrospective phylogenetic approaches.

Keywords: West Nile Virus, Dengue Virus, Rift Valley Fever Virus, Sindbis Virus, Mosquito Cell

Contributor Information

Esteban Domingo, Email: edomingo@cbm.uam.es.

S. C. Weaver, Email: sweaver@utmb.edu

References

  1. Armstrong P.M., Rico-Hesse R. Efficiency of dengue serotype 2 virus strains to infect and disseminate in Aedes aegypti. Am J Trop Med Hyg. 2003;68:539–544. doi: 10.4269/ajtmh.2003.68.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baldridge G.D., Beaty B.J., Hewlett M.J. Genomic stability of La Crosse virus during vertical and horizontal transmission. Arch Virol. 1989;108:89–99. doi: 10.1007/BF01313746. [DOI] [PubMed] [Google Scholar]
  3. Baric R.S., Yount B., Hensley L., Peel S.A., Chen W. Episodic evolution mediates interspecies transfer of a murine coronavirus. J Virol. 1997;71:1946–1955. doi: 10.1128/jvi.71.3.1946-1955.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beasley D.W., Davis C.T., Guzman H., Vanlandingham D.L., Travassos da Rosa A.P., Parsons R.E., Higgs S., Tesh R.B., Barrett A.D. Limited evolution of West Nile virus has occurred during its southwesterly spread in the United States. Virology. 2003;309:190–195. doi: 10.1016/S0042-6822(03)00150-8. [DOI] [PubMed] [Google Scholar]
  5. Bennett S.N., Holmes E.C., Chirivella M., Rodriguez D.M., Beltran M., Vorndam V., Gubler D.J., McMillan W.O. Selection-driven evolution of emergent dengue virus. Mol Biol Evol. 2003;20:1650–1658. doi: 10.1093/molbev/msg182. [DOI] [PubMed] [Google Scholar]
  6. Bilsel P.A., Tesh R.B., Nichol S.T. RNA genome stability of Toscana virus during serial transovarial transmission in the sandfly Phlebotomus perniciosus. Virus Res. 1988;11:87–94. doi: 10.1016/0168-1702(88)90069-X. [DOI] [PubMed] [Google Scholar]
  7. Bonneau K.R., Mullens B.A., MacLachlan N.J. Occurrence of genetic drift and founder effect during quasispecies evolution of the VP2 and NS3/NS3A genes of bluetongue virus upon passage between sheep, cattle, and Culicoides sonorensis. J Virol. 2001;75:8298–8305. doi: 10.1128/JVI.75.17.8298-8305.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Borucki M.K., Chandler L.J., Parker B.M., Blair C.D., Beaty B.J. Bunyavirus superinfection and segment reassortment in transovarially infected mosquitoes. J Gen Virol. 1999;80:3173–3179. doi: 10.1099/0022-1317-80-12-3173. [DOI] [PubMed] [Google Scholar]
  9. Bouloy M. Rift Valley fever virus. In: Service M.W., editor. The Encyclopedia of arthropod-transmitted Infections. Wallingford, UK: CAB International; 2001. pp. 426–434. [Google Scholar]
  10. Brault A.C. Pathology. Galveston, Texas: University of Texas Medical Branch; 2001. Genetic analysis of epizootic venezuelan equine encephalitis virus emergence mechanisms; p. 318. [Google Scholar]
  11. Brault A.C., Powers A.M., Chavez C.L., Lopez R.N., Cachon M.F., Gutierrez L.F., Kang W., Tesh R.B., Shope R.E., Weaver S.C. Genetic and antigenic diversity among eastern equine encephalitis viruses from North, Central, and South America. Am J Trop Med Hyg. 1999;61:579–586. doi: 10.4269/ajtmh.1999.61.579. [DOI] [PubMed] [Google Scholar]
  12. Brault A.C., Powers A.M., Holmes E.C., Woelk C.H., Weaver S.C. Positively charged amino acid substitutions in the E2 envelope glycoprotein are associated with the emergence of Venezuelan equine encephalitis virus. J Virol. 2002;76:1718–1730. doi: 10.1128/JVI.76.4.1718-1730.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Brault A.C., Powers A.M., Weaver S.C. Vector infection determinants of Venezuelan equine encephalitis virus reside within the E2 envelope glycoprotein. J Virol. 2002;76:6387–6392. doi: 10.1128/JVI.76.12.6387-6392.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Brault A.C., Powers A.M., Ortiz D., Estrada-Franco J.G., Navarro-Lopez R., Weaver S.C. Venezuelan equine encephalitis emergence: enhanced vector infection from a single amino acid substitution in the envelope glycoprotein. Proc Natl Acad Sci U S A. 2004;101:11344–11349. doi: 10.1073/pnas.0402905101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Bryant J., Wang H., Cabezas C., Ramirez G., Watts D., Russell K., Barrett A. Enzootic transmission of yellow fever virus in Peru. Emerg Infect Dis. 2003;9:926–933. doi: 10.3201/eid0908.030075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Byrnes A.P., Griffin D.E. Binding of Sindbis virus to cell surface heparan sulfate. J Virol. 1998;72:7349–7356. doi: 10.1128/jvi.72.9.7349-7356.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Calisher C.H., Karabatsos N. Arbovirus serogroups: definition and geographic distribution. In: Monath T.P., editor. The arboviruses: epidemiology and ecology. Boca Raton, FL: CRC Press; 1988. pp. 19–57. [Google Scholar]
  18. Chamberlain R.W., Kissling R.E., Sikes R.K. Studies on the North American arthropod-borne encephalitides. VII. Estimation of amount of eastern equine encephalitis virus inoculated by infected Aedes aegypti. Am J Hyg. 1954;60:286–291. [PubMed] [Google Scholar]
  19. Cilnis M.J., Kang W., Weaver S.C. Genetic conservation of Highlands J viruses. Virology. 1996;218:343–351. doi: 10.1006/viro.1996.0203. [DOI] [PubMed] [Google Scholar]
  20. Collins W.E. Transmission of Semliki Forest virus by Anopheles albimanus using membrane feeding techniques. Mosq News. 1963;23:96–99. [Google Scholar]
  21. Cooper L.A., Scott T.W. Differential evolution of eastern equine encephalitis virus populations in response to host cell type. Genetics. 2001;157:1403–1412. doi: 10.1093/genetics/157.4.1403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Craig S., Thu H.M., Lowry K., Wang X.F., Holmes E.C., Aaskov J. Diverse dengue type 2 virus populations contain recombinant and both parental viruses in a single mosquito host. J Virol. 2003;77:4463–4467. doi: 10.1128/JVI.77.7.4463-4467.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Crochu S., Cook S., Attoui H., Charrel R.N., De Chesse R., Belhouchet M., Lemasson J.J., de Micco P., de Lamballerie X. Sequences of flavivirus-related RNA viruses persist in DNA form integrated in the genome of Aedes spp. mosquitoes. J Gen Virol. 2004;85:1971–1980. doi: 10.1099/vir.0.79850-0. [DOI] [PubMed] [Google Scholar]
  24. Diallo M., Ba Y., Sall A.A., Diop O.M., Ndione J.A., Mondo M., Girault L., Mathiot C. Amplification of the sylvatic cycle of dengue virus type 2, Senegal, 1999–2000: entomologic findings and epidemiologic considerations. Emerg Infect Dis. 2003;9:362–367. doi: 10.3201/eid0903.020219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Duarte E., Clarke D., Moya A., Domingo E., Holland J. Rapid fitness losses in mammalian RNA virus clones due to Muller’s ratchet. Proc Natl Acad Sci U S A. 1992;89:6015–6019. doi: 10.1073/pnas.89.13.6015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. El Hussein A., Ramig R.F., Holbrook F.R., Beaty B.J. Asynchronous mixed infection of Culicoides variipennis with bluetongue virus serotypes 10 and 17. J Gen Virol. 1989;70:3355–3362. doi: 10.1099/0022-1317-70-12-3355. [DOI] [PubMed] [Google Scholar]
  27. Endy T.P., Nisalak A. Japanese encephalitis virus: ecology and epidemiology. Curr Top Microbiol Immunol. 2002;267:11–48. doi: 10.1007/978-3-642-59403-8_2. [DOI] [PubMed] [Google Scholar]
  28. Ferguson N., Anderson R., Gupta S. The effect of antibody-dependent enhancement on the transmission dynamics and persistence of multiple-strain pathogens. Proc Natl Acad Sci U S A. 1999;96:790–794. doi: 10.1073/pnas.96.2.790. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Gerrard S.R., Li L., Barrett A.D., Nichol S.T. Ngari virus is a Bunyamwera virus reassortant that can be associated with large outbreaks of hemorrhagic fever in Africa. J Virol. 2004;78:8922–8926. doi: 10.1128/JVI.78.16.8922-8926.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Gould E.A., de Lamballerie X., Zanotto P.M., Holmes E.C. Origins, evolution, and vector/host coadaptations within the genus Flavivirus. Adv Virus Res. 2003;59:277–314. doi: 10.1016/s0065-3527(03)59008-x. [DOI] [PubMed] [Google Scholar]
  31. Greene I.P., Paessler S., Austgen L., Anishchenko M., Brault A.C., Bowen R.A., Weaver S.C. Envelope glycoprotein mutations mediate equine amplification and virulence of epizootic Venezuelan equine encephalitis virus. J Virol. 2005;79:9128–9133. doi: 10.1128/JVI.79.14.9128-9133.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Greene IP, Wang E, Deardorff ER, Milleron R, Domingo E, Weaver SC (2005) Effect of alternating passage on adaptation of Sindbis virus to vertebrate and invertebrate cells. J Virol (in press) [DOI] [PMC free article] [PubMed]
  33. Griffin D.E. Alphaviruses. In: Knipe D.M., Howley P.M., editors. Fields’ virology. 4th edn. New York: Lippincott, Williams and Wilkins; 2001. pp. 917–962. [Google Scholar]
  34. Gubler D.J., Rosen L. A simple technique for demonstrating transmission of dengue virus by mosquitoes without the use of vertebrate hosts. Am J Trop Med Hyg. 1976;25:146–150. doi: 10.4269/ajtmh.1976.25.146. [DOI] [PubMed] [Google Scholar]
  35. Hahn C.S., Lustig S., Strauss E.G., Strauss J.H. Western equine encephalitis virus is a recombinant virus. Proc Natl Acad Sci U S A. 1988;85:5997–6001. doi: 10.1073/pnas.85.16.5997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Harrington L.C., Edman J.D., Scott T.W. Why do female Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood? J Med Entomol. 2001;38:411–422. doi: 10.1603/0022-2585-38.3.411. [DOI] [PubMed] [Google Scholar]
  37. Hertz J.M., Huang H.V. Utilization of heterologous alphavirus junction sequences as promoters by Sindbis virus. J Virol. 1992;66:857–864. doi: 10.1128/jvi.66.2.857-864.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Hertz J.M., Huang H.V. Evolution of the Sindbis virus subgenomic mRNA promoter in cultured cells. J Virol. 1995;69:7768–7774. doi: 10.1128/jvi.69.12.7768-7774.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Hertz J.M., Huang H.V. Host-dependent evolution of the Sindbis virus promoter for subgenomic mRNA synthesis. J Virol. 1995;69:7775–7781. doi: 10.1128/jvi.69.12.7775-7781.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Hilgard P., Stockert R. Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes. Hepatology. 2000;32:1069–1077. doi: 10.1053/jhep.2000.18713. [DOI] [PubMed] [Google Scholar]
  41. Holland J., Domingo E. Origin and evolution of viruses. Virus Genes. 1998;16:13–21. doi: 10.1023/A:1007989407305. [DOI] [PubMed] [Google Scholar]
  42. Holland J.J., Spindler K., Horodyski F., Grabau E., Nichol S., VandePol S. Rapid evolution of RNA genomes. Science. 1982;215:1577–1585. doi: 10.1126/science.7041255. [DOI] [PubMed] [Google Scholar]
  43. Holland J.J., de la Torre J.C., Clarke D.K., Duarte E. Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses. J Virol. 1991;65:2960–2967. doi: 10.1128/jvi.65.6.2960-2967.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Holmes E.C. Molecular clocks and the puzzle of RNA virus origins. J Virol. 2003;77:3893–3897. doi: 10.1128/JVI.77.7.3893-3897.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Holmes E.C., Twiddy S.S. The origin, emergence and evolutionary genetics of dengue virus. Infect Genet Evol. 2003;3:19–28. doi: 10.1016/S1567-1348(03)00004-2. [DOI] [PubMed] [Google Scholar]
  46. Hughes A.L. Evolutionary change of predicted cytotoxic T cell epitopes of dengue virus. Infect Genet Evol. 2001;1:123–130. doi: 10.1016/S1567-1348(01)00013-2. [DOI] [PubMed] [Google Scholar]
  47. Hurlbut H.S. Mosquito salivation and virus transmission. Am J Trop Med Hyg. 1966;15:989–993. doi: 10.4269/ajtmh.1966.15.989. [DOI] [PubMed] [Google Scholar]
  48. Jones L.D., Gaunt M., Hails R.S., Laurenson K., Hudson P.J., Reid H., Henbest P., Gould E.A. Transmission of louping ill virus between infected and uninfected ticks co-feeding on mountain hares. Med Vet Entomol. 1997;11:172–176. doi: 10.1111/j.1365-2915.1997.tb00309.x. [DOI] [PubMed] [Google Scholar]
  49. Karabatsos N. International catalogue of arboviruses. San Antonio: Am Soc Trop Med Hyg; 1985. [DOI] [PubMed] [Google Scholar]
  50. Karpf A.R., Lenches E., Strauss E.G., Strauss J.H., Brown D.T. Superinfection exclusion of alphaviruses in three mosquito cell lines persistently infected with Sindbis virus. J Virol. 1997;71:7119–7123. doi: 10.1128/jvi.71.9.7119-7123.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Klimstra W.B., Ryman K.D., Johnston R.E. Adaptation of Sindbis virus to BHK cells selects for use of heparan sulfate as an attachment receptor. J Virol. 1998;72:7357–7366. doi: 10.1128/jvi.72.9.7357-7366.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Kramer L.D., Chandler L.J. Phylogenetic analysis of the envelope gene of St. Louis encephalitis virus. Arch Virol. 2001;146:2341–2355. doi: 10.1007/s007050170007. [DOI] [PubMed] [Google Scholar]
  53. Lamotte L.C., Jr Japanese B encephalitis virus in the organs of infected mosquitoes. Am J Hyg. 1960;72:73–87. doi: 10.1093/oxfordjournals.aje.a120136. [DOI] [PubMed] [Google Scholar]
  54. Lin S.R., Hsieh S.C., Yueh Y.Y., Lin T.H., Chao D.Y., Chen W.J., King C.C., Wang W.K. Study of sequence variation of dengue type 3 virus in naturally infected mosquitoes and human hosts: implications for transmission and evolution. J Virol. 2004;78:12717–12721. doi: 10.1128/JVI.78.22.12717-12721.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Lindenbach B.D., Rice C.M. Flaviviridae: the viruses and their replication. In: Knipe D.M., Howley P.M., editors. Fields’ virology. 4th edn. New York: Lippincott, Williams and Wilkins; 2001. pp. 991–1041. [Google Scholar]
  56. Llewellyn Z.N., Salman M.D., Pauszek S., Rodriguez L.L. Growth and molecular evolution of vesicular stomatitis serotype New Jersey in cells derived from its natural insect-host: evidence for natural adaptation. Virus Res. 2002;89:65–73. doi: 10.1016/S0168-1702(02)00113-2. [DOI] [PubMed] [Google Scholar]
  57. Lobigs M., Marshall I.D., Weir R.C., Dalgarno L. Murray Valley encephalitis virus field strains from Australia and Papua New Guinea: studies on the sequence of the major envelope protein gene and virulence for mice. Virology. 1988;165:245–255. doi: 10.1016/0042-6822(88)90678-2. [DOI] [PubMed] [Google Scholar]
  58. Lopez S., Yao J.S., Kuhn R.J., Strauss E.G., Strauss J.H. Nucleocapsid-glycoprotein interactions required for assembly of alphaviruses. J Virol. 1994;68:1316–1323. doi: 10.1128/jvi.68.3.1316-1323.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Mackenzie J.S., Poidinger M., Lindsay M.D., Hall R.A., Sammels L.M. Molecular epidemiology and evolution of mosquito-borne flaviviruses and alphaviruses enzootic in Australia. Virus Genes. 1995;11:225–237. doi: 10.1007/BF01728662. [DOI] [PubMed] [Google Scholar]
  60. Mendez W., Liria J., Navarro J.C., Garcia C.Z., Freier J.E., Salas R., Weaver S.C., Barrera R. Spatial dispersion of adult mosquitoes (Diptera: Culicidae) in a sylvatic focus of Venezuelan equine encephalitis virus. J Med Entomol. 2001;38:813–821. doi: 10.1603/0022-2585-38.6.813. [DOI] [PubMed] [Google Scholar]
  61. Moncayo A.C., Fernandez Z., Diallo M., Ortiz D., Sall A., Hartman S., Davis C.T., Coffey L.L., Mathiot C.C., Tesh R.B., Weaver S.C. Dengue emergence and adaptation to peridomestic mosquitoes. Emerg Infect Dis. 2004;10:1790–1796. doi: 10.3201/eid1010.030846. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Morzunov S.P., Rowe J.E., Ksiazek T.G., Peters C.J., St. Jeor S.C., Nichol S.T. Genetic analysis of the diversity and origin of hantaviruses in Peromyscus leucopus mice in North America. J Virol. 1998;72:57–64. doi: 10.1128/jvi.72.1.57-64.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Navarro J.C., Weaver S.C. Molecular phylogeny of the Vomerifer and Pedroi groups in the Spissipes section of the subgenus Culex (Melanoconion) J Med Entomol. 2004;41:575–581. doi: 10.1603/0022-2585-41.4.575. [DOI] [PubMed] [Google Scholar]
  64. Norder H., Lundstrom J.O., Kozuch O., Magnius L.O. Genetic relatedness of Sindbis virus strains from Europe, Middle East, and Africa. Virology. 1996;222:440–445. doi: 10.1006/viro.1996.0441. [DOI] [PubMed] [Google Scholar]
  65. Novella I.S., Clarke D.K., Quer J., Duarte E.A., Lee C.H., Weaver S.C., Elena S.F., Moya A., Domingo E., Holland J.J. Extreme fitness differences in mammalian and insect hosts after continuous replication of vesicular stomatitis virus in sandfly cells. J Virol. 1995;69:6805–6809. doi: 10.1128/jvi.69.11.6805-6809.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Novella I.S., Hershey C.L., Escarmis C., Domingo E., Holland J.J. Lack of evolutionary stasis during alternating replication of an arbovirus in insect and mammalian cells. J Mol Biol. 1999;287:459–465. doi: 10.1006/jmbi.1999.2635. [DOI] [PubMed] [Google Scholar]
  67. Ortiz D.I., Weaver S.C. Susceptibility of Ochlerotatus taeniorhynchus (Diptera: Culicidae) to infection with epizootic (subtype IC) and enzootic (subtype ID) Venezuelan Equine encephalitis viruses: evidence for epizootic strain adaptation. J Med Entomol. 2004;41:987–993. doi: 10.1603/0022-2585-41.5.987. [DOI] [PubMed] [Google Scholar]
  68. Poidinger M., Roy S., Hall R.A., Turley P.J., Scherret J.H., Lindsay M.D., Broom A.K., Mackenzie J.S. Genetic stability among temporally and geographically diverse isolates of Barmah Forest virus. Am J Trop Med Hyg. 1997;57:230–234. doi: 10.4269/ajtmh.1997.57.230. [DOI] [PubMed] [Google Scholar]
  69. Powers A.M., Brault A.C., Tesh R.B., Weaver S.C. Re-emergence of Chikungunya and O’nyong-nyong viruses: evidence for distinct geographical lineages and distant evolutionary relationships. J Gen Virol. 2000;81:471–479. doi: 10.1099/0022-1317-81-2-471. [DOI] [PubMed] [Google Scholar]
  70. Powers A.M., Brault A.C., Shirako Y., Strauss E.G., Kang W., Strauss J.H., Weaver S.C. Evolutionary relationships and systematics of the alphaviruses. J Virol. 2001;75:10118–10131. doi: 10.1128/JVI.75.21.10118-10131.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Ross R.W. Annual Report. Entebbe, Uganda: Research Institute; 1955. A laboratory technique for studying the insect transmission of animal viruses, employing abat-wingmembrane, demonstrated with two African viruses; pp. 192–200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Rudnick A. The ecology of the dengue virus complex in Peninsular Malaysia. In: Pang T., Pathmanathan R., editors. Proceedings of the International Conference on Dengue/DHF. Kuala Lumpur: University of Malaysia Press; 1984. p. 7. [Google Scholar]
  73. Ruiz-Jarabo C.M., Pariente N., Baranowski E., Davila M., Gomez-Mariano G., Domingo E. Expansion of host-cell tropism of foot-and-mouth disease virus despite replication in a constant environment. J Gen Virol. 2004;85:2289–2297. doi: 10.1099/vir.0.80126-0. [DOI] [PubMed] [Google Scholar]
  74. Sammels L.M., Coelen R.J., Lindsay M.D., Mackenzie J.S. Geographic distribution and evolution of Ross River virus in Australia and the Pacific Islands. Virology. 1995;212:20–29. doi: 10.1006/viro.1995.1449. [DOI] [PubMed] [Google Scholar]
  75. Sammels L.M., Lindsay M.D., Poidinger M., Coelen R.J., Mackenzie J.S. Geographic distribution and evolution of Sindbis virus in Australia. J Gen Virol. 1999;80:739–748. doi: 10.1099/0022-1317-80-3-739. [DOI] [PubMed] [Google Scholar]
  76. Schlesinger S., Schlesinger M.J. Togaviridae: The viruses and their replication. In: Howley P.M., editor. Fields’ virology. 4th edn. New York: Lippincott, Williams and Wilkins; 2001. pp. 895–916. [Google Scholar]
  77. Scott T.W., Weaver S.C. Eastern equine encephalomyelitis virus: epidemiology and evolution of mosquito transmission. Adv Virus Res. 1989;37:277–328. doi: 10.1016/s0065-3527(08)60838-6. [DOI] [PubMed] [Google Scholar]
  78. Shiu S.Y., Ayres M.D., Gould E.A. Genomic sequence of the structural proteins of louping ill virus: comparative analysis with tick-borne encephalitis virus. Virology. 1991;180:411–415. doi: 10.1016/0042-6822(91)90048-G. [DOI] [PubMed] [Google Scholar]
  79. Simmonds P., Tuplin A., Evans D.J. Detection of genome-scale ordered RNA structure (GORS) in genomes of positive-stranded RNA viruses: implications for virus evolution and host persistence. RNA. 2004;10:1337–1351. doi: 10.1261/rna.7640104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Smith D.R., Carrara A.S., Aguilar P.V., Weaver S.C. Evaluation of methods to assess transmission potential of Venezuelan equine encephalitis virus by mosquitoes and estimation of mosquito saliva titers. Am J Trop Med Hyg. 2005;73:33–39. [PubMed] [Google Scholar]
  81. Solomon T., Ni H., Beasley D.W., Ekkelenkamp M., Cardosa M.J., Barrett A.D. Origin and evolution of Japanese encephalitis virus in southeast Asia. J Virol. 2003;77:3091–3098. doi: 10.1128/JVI.77.5.3091-3098.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Strauss J.H., Strauss E.G. The alphaviruses: gene expression, replication, and evolution. Microbiol Rev. 1994;58:491–562. doi: 10.1128/mr.58.3.491-562.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Tabachnick W.J., Powell J.R. Aworld-wide survey of genetic variation in the yellow fever mosquito, Aedes aegypti. Genet Res. 1979;34:215–229. doi: 10.1017/s0016672300019467. [DOI] [PubMed] [Google Scholar]
  84. Taylor W.P., Marshall I.D. Adaptation studies with Ross River virus: laboratory mice and cell cultures. J Gen Virol. 1975;28:59–72. doi: 10.1099/0022-1317-28-1-59. [DOI] [PubMed] [Google Scholar]
  85. Taylor W.P., Marshall I.D. Adaptation studies with Ross River virus: retention of field level virulence. J Gen Virol. 1975;28:73–83. doi: 10.1099/0022-1317-28-1-73. [DOI] [PubMed] [Google Scholar]
  86. Thu H.M., Lowry K., Myint T.T., Shwe T.N., Han A.M., Khin K.K., Thant K.Z., Thein S., Aaskov J. Myanmar dengue outbreak associated with displacement of serotypes 2, 3, and 4 by dengue 1. Emerg Infect Dis. 2004;10:593–597. doi: 10.3201/eid1004.030216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Tsai T.F., Weaver S.C., Monath T.P. Alphaviruses. In: Richman D.D., Whitley R.J., Hayden F.G., editors. Clinical virology. Washington, DC: ASM Press; 2002. pp. 1177–1210. [Google Scholar]
  88. Turell M.J., Sardelis M.R., O’Guinn M.L., Dohm D.J. Potential vectors of West Nile virus in North America. Curr Top Microbiol Immunol. 2002;267:241–252. doi: 10.1007/978-3-642-59403-8_12. [DOI] [PubMed] [Google Scholar]
  89. Twiddy S.S., Farrar J.J., Vinh Chau N., Wills B., Gould E.A., Gritsun T., Lloyd G., Holmes E.C. Phylogenetic relationships and differential selection pressures among genotypes of dengue-2 virus. Virology. 2002;298:63–72. doi: 10.1006/viro.2002.1447. [DOI] [PubMed] [Google Scholar]
  90. Twiddy S.S., Woelk C.H., Holmes E.C. Phylogenetic evidence for adaptive evolution of dengue viruses in nature. J Gen Virol. 2002;83:1679–1689. doi: 10.1099/0022-1317-83-7-1679. [DOI] [PubMed] [Google Scholar]
  91. Van Regenmortel MHV, Fauquet CM, Bishop DHL, Carstens EB, Estes MK, Lemon SM, Maniloff J, Mayo MA, McGeogh DJ, Pringle CR, Wickner RB (eds) (2000) Virus taxonomy. Classification and nomenclature of viruses. Seventh report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego
  92. Vanlandingham D.L., Schneider B.S., Klingler K., Fair J., Beasley D., Huang J., Hamilton P., Higgs S. Real-time reverse transcriptase-polymerase chain reaction quantification of West Nile virus transmitted by Culex Pipiens Quinquefasciatus. Am J Trop Med Hyg. 2004;71:120–123. [PubMed] [Google Scholar]
  93. Wang E., Ni H., Xu R., Barrett A.D., Watowich S.J., Gubler D.J., Weaver S.C. Evolutionary relationships of endemic/epidemic and sylvatic dengue viruses. J Virol. 2000;74:3227–3234. doi: 10.1128/jvi.74.7.3227-3234.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Watts D.M., Porter K.R., Putvatana P., Vasquez B., Calampa C., Hayes C.G., Halstead S.B. Failure of secondary infection with American genotype dengue 2 to cause dengue haemorrhagic fever. Lancet. 1999;354:1431–1434. doi: 10.1016/S0140-6736(99)04015-5. [DOI] [PubMed] [Google Scholar]
  95. Weaver S.C. Evolution of alphaviruses. In: Gibbs A.J., Calisher C.H., Garcia-Arenal F., editors. Molecular basis of virus evolution. Cambridge: Cambridge University Press; 1995. pp. 501–530. [Google Scholar]
  96. Weaver S.C., Barrett A.D. Transmission cycles, host range, evolution and emergence of arboviral disease. Nat Rev Microbiol. 2004;2:789–801. doi: 10.1038/nrmicro1006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. Weaver S.C., Scott T.W., Lorenz L.H. Patterns of eastern equine encephalomyelitis virus infection in Culiseta melanura (Diptera: Culicidae) JMed Entomol. 1990;27:878–891. doi: 10.1093/jmedent/27.5.878. [DOI] [PubMed] [Google Scholar]
  98. Weaver S.C., Rico-Hesse R., Scott T.W. Genetic diversity and slow rates of evolution in New World alphaviruses. Curr Topics Microbiol Immunol. 1992;176:99–117. doi: 10.1007/978-3-642-77011-1_7. [DOI] [PubMed] [Google Scholar]
  99. Weaver S.C., Bellew L.A., Gousset L., Repik P.M., Scott T.W., Holland J.J. Diversity within natural populations of eastern equine encephalomyelitis virus. Virology. 1993;195:700–709. doi: 10.1006/viro.1993.1421. [DOI] [PubMed] [Google Scholar]
  100. Weaver S.C., Kang W., Shirako Y., Rumenapf T., Strauss E.G., Strauss J.H. Recombinational history and molecular evolution of western equine encephalomyelitis complex alphaviruses. J Virol. 1997;71:613–623. doi: 10.1128/jvi.71.1.613-623.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Weaver S.C., Brault A.C., Kang W., Holland J.J. Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J Virol. 1999;73:4316–4326. doi: 10.1128/jvi.73.5.4316-4326.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. Weaver S.C., Dalgarno L., Frey T.K., Huang H.V., Kinney R.M., Rice C.M., Roehrig J.T., Shope R.E., Strauss E.G. Family Togaviridae. In: van Regenmortel M.H.V., Fauquet C.M., Bishop D.H.L., Carstens E.B., Estes M.K., Lemon S.M., Maniloff J., Mayo M.A., McGeogh D.J., Pringle C.R., Wickner R.B., editors. Virus taxonomy. Classification and nomenclature of viruses. San Diego: Academic Press; 2000. pp. 879–889. [Google Scholar]
  103. Weaver S.C., Anishchenko M., Bowen R., Brault A.C., Estrada-Franco J.G., Fernandez Z., Greene I., Ortiz D., Paessler S., Powers A.M. Genetic determinants of Venezuelan equine encephalitis emergence. Arch Virol. 2004;Suppl:43–64. doi: 10.1007/978-3-7091-0572-6_5. [DOI] [PubMed] [Google Scholar]
  104. Weaver S.C., Ferro C., Barrera R., Boshell J., Navarro J.C. Venezuelan equine encephalitis. Annu Rev Entomol. 2004;49:141–174. doi: 10.1146/annurev.ento.49.061802.123422. [DOI] [PubMed] [Google Scholar]
  105. Woodall J. Chikungunya virus. In: Service M.W., editor. The encyclopedia of arthropod-transmitted infections. Wallingford, UK: CAB International; 2001. pp. 115–119. [Google Scholar]
  106. Zanotto P.M., Gao G.F., Gritsun T., Marin M.S., Jiang W.R., Venugopal K., Reid H.W., Gould E.A. An arbovirus cline across the northern hemisphere. Virology. 1995;210:152–159. doi: 10.1006/viro.1995.1326. [DOI] [PubMed] [Google Scholar]
  107. Zanotto P.M., Gould E.A., Gao G.F., Harvey P.H., Holmes E.C. Population dynamics of flaviviruses revealed by molecular phylogenies. Proc Natl Acad Sci U S A. 1996;93:548–553. doi: 10.1073/pnas.93.2.548. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Quasispecies: Concept and Implications for Virology are provided here courtesy of Nature Publishing Group

RESOURCES