Evolutionary Influences in Arboviral Disease

  • S. C. Weaver
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 299)


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.


West Nile Virus Dengue Virus Rift Valley Fever Virus Sindbis Virus Mosquito Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Armstrong PM, Rico-Hesse R (2003) Efficiency of dengue serotype 2 virus strains to infect and disseminate in Aedes aegypti. Am J Trop Med Hyg 68:539–544PubMedGoogle Scholar
  2. Baldridge GD, Beaty BJ, Hewlett MJ (1989) Genomic stability of La Crosse virus during vertical and horizontal transmission. Arch Virol 108:89–99CrossRefPubMedGoogle Scholar
  3. Baric RS, Yount B, Hensley L, Peel SA, Chen W (1997) Episodic evolution mediates interspecies transfer of a murine coronavirus. J Virol 71:1946–1955PubMedGoogle Scholar
  4. Beasley DW, Davis CT, Guzman H, Vanlandingham DL, Travassos da Rosa AP, Parsons RE, Higgs S, Tesh RB, Barrett AD (2003) Limited evolution of West Nile virus has occurred during its southwesterly spread in the United States. Virology 309:190–195CrossRefPubMedGoogle Scholar
  5. Bennett SN, Holmes EC, Chirivella M, Rodriguez DM, Beltran M, Vorndam V, Gubler DJ, McMillan WO (2003) Selection-driven evolution of emergent dengue virus. Mol Biol Evol 20:1650–1658PubMedGoogle Scholar
  6. Bilsel PA, Tesh RB, Nichol ST (1988) RNA genome stability of Toscana virus during serial transovarial transmission in the sandfly Phlebotomus perniciosus. Virus Res 11:87–94CrossRefPubMedGoogle Scholar
  7. Bonneau KR, Mullens BA, MacLachlan NJ (2001) 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 75:8298–8305CrossRefPubMedGoogle Scholar
  8. Borucki MK, Chandler LJ, Parker BM, Blair CD, Beaty BJ (1999) Bunyavirus superinfection and segment reassortment in transovarially infected mosquitoes. J Gen Virol 80:3173–3179PubMedGoogle Scholar
  9. Bouloy M (2001) Rift Valley fever virus. In: Service MW (ed) The Encyclopedia of arthropod-transmitted Infections. CAB International, Wallingford, UK, pp 426–434Google Scholar
  10. Brault AC (2001) Genetic analysis of epizootic venezuelan equine encephalitis virus emergence mechanisms. In: Pathology. University of Texas Medical Branch, Galveston, Texas, p 318Google Scholar
  11. Brault AC, Powers AM, Chavez CL, Lopez RN, Cachon MF, Gutierrez LF, Kang W, Tesh RB, Shope RE, Weaver SC (1999) Genetic and antigenic diversity among eastern equine encephalitis viruses from North, Central, and South America. Am J Trop Med Hyg 61:579–586PubMedGoogle Scholar
  12. Brault AC, Powers AM, Holmes EC, Woelk CH, Weaver SC (2002a) Positively charged amino acid substitutions in the E2 envelope glycoprotein are associated with the emergence of Venezuelan equine encephalitis virus. J Virol 76:1718–1730PubMedGoogle Scholar
  13. Brault AC, Powers AM, Weaver SC (2002b) Vector infection determinants of Venezuelan equine encephalitis virus reside within the E2 envelope glycoprotein. J Virol 76:6387–6392PubMedGoogle Scholar
  14. Brault AC, Powers AM, Ortiz D, Estrada-Franco JG, Navarro-Lopez R, Weaver SC (2004) Venezuelan equine encephalitis emergence: enhanced vector infection from a single amino acid substitution in the envelope glycoprotein. Proc Natl Acad Sci U S A 101:11344–11349CrossRefPubMedGoogle Scholar
  15. Bryant J, Wang H, Cabezas C, Ramirez G, Watts D, Russell K, Barrett A (2003) Enzootic transmission of yellow fever virus in Peru. Emerg Infect Dis 9:926–933PubMedGoogle Scholar
  16. Byrnes AP, Griffin DE (1998) Binding of Sindbis virus to cell surface heparan sulfate. J Virol 72:7349–7356PubMedGoogle Scholar
  17. Calisher CH, Karabatsos N (1988) Arbovirus serogroups: definition and geographic distribution. In: Monath TP (ed) The arboviruses: epidemiology and ecology. Vol. I. CRC Press, Boca Raton, FL, pp 19–57Google Scholar
  18. Chamberlain RW, Kissling RE, Sikes RK (1954) 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 60:286–291PubMedGoogle Scholar
  19. Cilnis MJ, Kang W, Weaver SC (1996) Genetic conservation of Highlands J viruses. Virology 218:343–351CrossRefPubMedGoogle Scholar
  20. Collins WE (1963) Transmission of Semliki Forest virus by Anopheles albimanus using membrane feeding techniques. Mosq News 23:96–99Google Scholar
  21. Cooper LA, Scott TW(2001) Differential evolution of eastern equine encephalitis virus populations in response to host cell type. Genetics 157:1403–1412PubMedGoogle Scholar
  22. Craig S, Thu HM, Lowry K, Wang XF, Holmes EC, Aaskov J (2003) Diverse dengue type 2 virus populations contain recombinant and both parental viruses in a single mosquito host. J Virol 77:4463–4467CrossRefPubMedGoogle Scholar
  23. Crochu S, Cook S, Attoui H, Charrel RN, De Chesse R, Belhouchet M, Lemasson JJ, 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 85:1971–1980CrossRefPubMedGoogle Scholar
  24. Diallo M, Ba Y, Sall AA, Diop OM, Ndione JA, Mondo M, Girault L, Mathiot C (2003) Amplification of the sylvatic cycle of dengue virus type 2, Senegal, 1999–2000: entomologic findings and epidemiologic considerations. Emerg Infect Dis 9:362–367PubMedGoogle Scholar
  25. Duarte E, Clarke D, Moya A, Domingo E, Holland J (1992) Rapid fitness losses in mammalian RNA virus clones due to Muller’s ratchet. Proc Natl Acad Sci U S A 89:6015–6019PubMedGoogle Scholar
  26. El Hussein A, Ramig RF, Holbrook FR, Beaty BJ (1989) Asynchronous mixed infection of Culicoides variipennis with bluetongue virus serotypes 10 and 17. J Gen Virol 70:3355–3362PubMedGoogle Scholar
  27. Endy TP, Nisalak A (2002) Japanese encephalitis virus: ecology and epidemiology. Curr Top Microbiol Immunol 267:11–48PubMedGoogle Scholar
  28. Ferguson N, Anderson R, Gupta S (1999) The effect of antibody-dependent enhancement on the transmission dynamics and persistence of multiple-strain pathogens. Proc Natl Acad Sci U S A 96:790–794PubMedGoogle Scholar
  29. Gerrard SR, Li L, Barrett AD, Nichol ST (2004) Ngari virus is a Bunyamwera virus reassortant that can be associated with large outbreaks of hemorrhagic fever in Africa. J Virol 78:8922–8926CrossRefPubMedGoogle Scholar
  30. Gould EA, de Lamballerie X, Zanotto PM, Holmes EC (2003) Origins, evolution, and vector/host coadaptations within the genus Flavivirus. Adv Virus Res 59:277–314PubMedGoogle Scholar
  31. Greene IP, Paessler S, Austgen L, Anishchenko M, Brault AC, Bowen RA, Weaver SC (2005) Envelope glycoprotein mutations mediate equine amplification and virulence of epizootic Venezuelan equine encephalitis virus. J Virol 79: 9128–9133PubMedGoogle 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)Google Scholar
  33. Griffin DE (2001) Alphaviruses. In: Knipe DM, Howley PM (eds) Fields’ virology, 4th edn. Lippincott, Williams and Wilkins, New York, 917–962Google Scholar
  34. Gubler DJ, Rosen L (1976) A simple technique for demonstrating transmission of dengue virus by mosquitoes without the use of vertebrate hosts. Am J Trop Med Hyg 25:146–150PubMedGoogle Scholar
  35. Hahn CS, Lustig S, Strauss EG, Strauss JH (1988) Western equine encephalitis virus is a recombinant virus. Proc Natl Acad Sci U S A 85:5997–6001PubMedGoogle Scholar
  36. Harrington LC, Edman JD, Scott TW (2001) Why do female Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood? J Med Entomol 38:411–422PubMedGoogle Scholar
  37. Hertz JM, Huang HV (1992) Utilization of heterologous alphavirus junction sequences as promoters by Sindbis virus. J Virol 66:857–864PubMedGoogle Scholar
  38. Hertz JM, Huang HV (1995a) Evolution of the Sindbis virus subgenomic mRNA promoter in cultured cells. J Virol 69:7768–7774PubMedGoogle Scholar
  39. Hertz JM, Huang HV (1995b) Host-dependent evolution of the Sindbis virus promoter for subgenomic mRNA synthesis. J Virol 69:7775–7781PubMedGoogle Scholar
  40. Hilgard P, Stockert R (2000) Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes. Hepatology 32:1069–1077CrossRefPubMedGoogle Scholar
  41. Holland J, Domingo E (1998) Origin and evolution of viruses. Virus Genes 16:13–21CrossRefPubMedGoogle Scholar
  42. Holland JJ, Spindler K, Horodyski F, Grabau E, Nichol S, VandePol S (1982) Rapid evolution of RNA genomes. Science 215:1577–1585PubMedGoogle Scholar
  43. Holland JJ, de la Torre JC, Clarke DK, Duarte E (1991) Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses. J Virol 65:2960–2967PubMedGoogle Scholar
  44. Holmes EC (2003) Molecular clocks and the puzzle of RNA virus origins. J Virol 77:3893–3897PubMedGoogle Scholar
  45. Holmes EC, Twiddy SS (2003) The origin, emergence and evolutionary genetics of dengue virus. Infect Genet Evol 3:19–28CrossRefPubMedGoogle Scholar
  46. Hughes AL (2001) Evolutionary change of predicted cytotoxic T cell epitopes of dengue virus. Infect Genet Evol 1:123–130CrossRefPubMedGoogle Scholar
  47. Hurlbut HS (1966) Mosquito salivation and virus transmission. Am J Trop Med Hyg 15:989–993PubMedGoogle Scholar
  48. Jones LD, Gaunt M, Hails RS, Laurenson K, Hudson PJ, Reid H, Henbest P, Gould EA (1997) Transmission of louping ill virus between infected and uninfected ticks co-feeding on mountain hares. Med Vet Entomol 11:172–176PubMedGoogle Scholar
  49. Karabatsos N (1985) International catalogue of arboviruses. Am Soc Trop Med Hyg, San AntonioGoogle Scholar
  50. Karpf AR, Lenches E, Strauss EG, Strauss JH, Brown DT (1997) Superinfection exclusion of alphaviruses in three mosquito cell lines persistently infected with Sindbis virus. J Virol 71:7119–7123.PubMedGoogle Scholar
  51. Klimstra WB, Ryman KD, Johnston RE (1998) Adaptation of Sindbis virus to BHK cells selects for use of heparan sulfate as an attachment receptor. J Virol 72:7357–7366PubMedGoogle Scholar
  52. Kramer LD, Chandler LJ (2001) Phylogenetic analysis of the envelope gene of St. Louis encephalitis virus. Arch Virol 146:2341–2355CrossRefPubMedGoogle Scholar
  53. Lamotte LC Jr (1960) Japanese B encephalitis virus in the organs of infected mosquitoes. Am J Hyg 72:73–87PubMedGoogle Scholar
  54. Lin SR, Hsieh SC, Yueh YY, Lin TH, Chao DY, Chen WJ, King CC, Wang WK (2004) Study of sequence variation of dengue type 3 virus in naturally infected mosquitoes and human hosts: implications for transmission and evolution. J Virol 78:12717–12721PubMedGoogle Scholar
  55. Lindenbach BD, Rice CM (2001) Flaviviridae: the viruses and their replication. In: Knipe DM, Howley PM (eds) Fields’ virology, 4th edn. Lippincott, Williams and Wilkins, New York, 991–1041Google Scholar
  56. Llewellyn ZN, Salman MD, Pauszek S, Rodriguez LL (2002) Growth and molecular evolution of vesicular stomatitis serotype New Jersey in cells derived from its natural insect-host: evidence for natural adaptation. Virus Res 89: 65–73CrossRefPubMedGoogle Scholar
  57. Lobigs M, Marshall ID, Weir RC, Dalgarno L (1988) 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 165:245–255CrossRefPubMedGoogle Scholar
  58. Lopez S, Yao JS, Kuhn RJ, Strauss EG, Strauss JH (1994) Nucleocapsid-glycoprotein interactions required for assembly of alphaviruses. J Virol 68:1316–1323PubMedGoogle Scholar
  59. Mackenzie JS, Poidinger M, Lindsay MD, Hall RA, Sammels LM (1995) Molecular epidemiology and evolution of mosquito-borne flaviviruses and alphaviruses enzootic in Australia. Virus Genes 11:225–237CrossRefPubMedGoogle Scholar
  60. Mendez W, Liria J, Navarro JC, Garcia CZ, Freier JE, Salas R, Weaver SC, Barrera R (2001) Spatial dispersion of adult mosquitoes (Diptera: Culicidae) in a sylvatic focus of Venezuelan equine encephalitis virus. J Med Entomol 38:813–821PubMedGoogle Scholar
  61. Moncayo AC, Fernandez Z, Diallo M, Ortiz D, Sall A, Hartman S, Davis CT, Coffey LL, Mathiot CC, Tesh RB, Weaver SC (2004) Dengue emergence and adaptation to peridomestic mosquitoes. Emerg Infect Dis 10:1790–1796PubMedGoogle Scholar
  62. Morzunov SP, Rowe JE, Ksiazek TG, Peters CJ, St. Jeor SC, Nichol ST (1998) Genetic analysis of the diversity and origin of hantaviruses in Peromyscus leucopus mice in North America. J Virol 72:57–64PubMedGoogle Scholar
  63. Navarro JC, Weaver SC (2004) Molecular phylogeny of the Vomerifer and Pedroi groups in the Spissipes section of the subgenus Culex (Melanoconion). J Med Entomol 41:575–581PubMedGoogle Scholar
  64. Norder H, Lundstrom JO, Kozuch O, Magnius LO (1996) Genetic relatedness of Sindbis virus strains from Europe, Middle East, and Africa. Virology 222:440–445CrossRefPubMedGoogle Scholar
  65. Novella IS, Clarke DK, Quer J, Duarte EA, Lee CH, Weaver SC, Elena SF, Moya A, Domingo E, Holland JJ (1995) Extreme fitness differences in mammalian and insect hosts after continuous replication of vesicular stomatitis virus in sandfly cells. J Virol 69:6805–6809PubMedGoogle Scholar
  66. Novella IS, Hershey CL, Escarmis C, Domingo E, Holland JJ (1999) Lack of evolutionary stasis during alternating replication of an arbovirus in insect and mammalian cells. J Mol Biol 287:459–465CrossRefPubMedGoogle Scholar
  67. Ortiz DI, Weaver SC (2004) 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 41:987–993PubMedGoogle Scholar
  68. Poidinger M, Roy S, Hall RA, Turley PJ, Scherret JH, Lindsay MD, Broom AK, Mackenzie JS (1997) Genetic stability among temporally and geographically diverse isolates of Barmah Forest virus. Am J Trop Med Hyg 57:230–234PubMedGoogle Scholar
  69. Powers AM, Brault AC, Tesh RB, Weaver SC (2000) Re-emergence of Chikungunya and O’nyong-nyong viruses: evidence for distinct geographical lineages and distant evolutionary relationships. J Gen Virol 81:471–479PubMedGoogle Scholar
  70. Powers AM, Brault AC, Shirako Y, Strauss EG, Kang W, Strauss JH, Weaver SC (2001) Evolutionary relationships and systematics of the alphaviruses. J Virol 75:10118–10131CrossRefPubMedGoogle Scholar
  71. Ross RW (1955) A laboratory technique for studying the insect transmission of animal viruses, employing abat-wingmembrane, demonstrated with two African viruses. In: Annual Report, Virus Research Institute, Entebbe, Uganda, pp 192–200Google Scholar
  72. Rudnick A (1984) The ecology of the dengue virus complex in Peninsular Malaysia. In: Pang T, Pathmanathan R (eds) Proceedings of the International Conference on Dengue/DHF. University of Malaysia Press, Kuala Lumpur, p 7Google Scholar
  73. Ruiz-Jarabo CM, Pariente N, Baranowski E, Davila M, Gomez-Mariano G, Domingo E (2004) Expansion of host-cell tropism of foot-and-mouth disease virus despite replication in a constant environment. J Gen Virol 85:2289–2297CrossRefPubMedGoogle Scholar
  74. Sammels LM, Coelen RJ, Lindsay MD, Mackenzie JS (1995) Geographic distribution and evolution of Ross River virus in Australia and the Pacific Islands. Virology 212:20–29CrossRefPubMedGoogle Scholar
  75. Sammels LM, Lindsay MD, Poidinger M, Coelen RJ, Mackenzie JS (1999) Geographic distribution and evolution of Sindbis virus in Australia. J Gen Virol 80:739–748PubMedGoogle Scholar
  76. Schlesinger S, Schlesinger MJ (2001) Togaviridae: The viruses and their replication. In: Howley PM (ed) Fields’ virology, 4th edn. Lippincott, Williams and Wilkins, New York, 895–916Google Scholar
  77. Scott TW, Weaver SC (1989) Eastern equine encephalomyelitis virus: epidemiology and evolution of mosquito transmission. Adv Virus Res 37:277–328PubMedGoogle Scholar
  78. Shiu SY, Ayres MD, Gould EA (1991) Genomic sequence of the structural proteins of louping ill virus: comparative analysis with tick-borne encephalitis virus. Virology 180:411–415CrossRefPubMedGoogle Scholar
  79. Simmonds P, Tuplin A, Evans DJ (2004) Detection of genome-scale ordered RNA structure (GORS) in genomes of positive-stranded RNA viruses: implications for virus evolution and host persistence. RNA 10:1337–1351CrossRefPubMedGoogle Scholar
  80. Smith DR, Carrara AS, Aguilar PV, Weaver SC (2005) 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 73:33–39PubMedGoogle Scholar
  81. Solomon T, Ni H, Beasley DW, Ekkelenkamp M, Cardosa MJ, Barrett AD (2003) Origin and evolution of Japanese encephalitis virus in southeast Asia. J Virol 77:3091–3098CrossRefPubMedGoogle Scholar
  82. Strauss JH, Strauss EG (1994) The alphaviruses: gene expression, replication, and evolution. Microbiol Rev 58:491–562PubMedGoogle Scholar
  83. Tabachnick WJ, Powell JR (1979) Aworld-wide survey of genetic variation in the yellow fever mosquito, Aedes aegypti. Genet Res 34:215–229PubMedGoogle Scholar
  84. Taylor WP, Marshall ID (1975a) Adaptation studies with Ross River virus: laboratory mice and cell cultures. J Gen Virol 28:59–72PubMedGoogle Scholar
  85. Taylor WP, Marshall ID (1975b) Adaptation studies with Ross River virus: retention of field level virulence. J Gen Virol 28:73–83PubMedGoogle Scholar
  86. Thu HM, Lowry K, Myint TT, Shwe TN, Han AM, Khin KK, Thant KZ, Thein S, Aaskov J (2004) Myanmar dengue outbreak associated with displacement of serotypes 2, 3, and 4 by dengue 1. Emerg Infect Dis 10:593–597PubMedGoogle Scholar
  87. Tsai TF, Weaver SC, Monath TP (2002) Alphaviruses. In: Richman DD, Whitley RJ, Hayden FG (eds) Clinical virology. ASM Press, Washington, DC, pp 1177–1210Google Scholar
  88. Turell MJ, Sardelis MR, O’Guinn ML, Dohm DJ (2002) Potential vectors of West Nile virus in North America. Curr Top Microbiol Immunol 267:241–252PubMedGoogle Scholar
  89. Twiddy SS, Farrar JJ, Vinh Chau N, Wills B, Gould EA, Gritsun T, Lloyd G, Holmes EC (2002a) Phylogenetic relationships and differential selection pressures among genotypes of dengue-2 virus. Virology 298:63–72CrossRefPubMedGoogle Scholar
  90. Twiddy SS, Woelk CH, Holmes EC (2002b) Phylogenetic evidence for adaptive evolution of dengue viruses in nature. J Gen Virol 83:1679–1689PubMedGoogle 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 DiegoGoogle Scholar
  92. Vanlandingham DL, Schneider BS, Klingler K, Fair J, Beasley D, Huang J, Hamilton P, Higgs S (2004) Real-time reverse transcriptase-polymerase chain reaction quantification of West Nile virus transmitted by Culex Pipiens Quinquefasciatus. Am J Trop Med Hyg 71:120–123PubMedGoogle Scholar
  93. Wang E, Ni H, Xu R, Barrett AD, Watowich SJ, Gubler DJ, Weaver SC (2000) Evolutionary relationships of endemic/epidemic and sylvatic dengue viruses. J Virol 74:3227–3234PubMedGoogle Scholar
  94. Watts DM, Porter KR, Putvatana P, Vasquez B, Calampa C, Hayes CG, Halstead SB (1999) Failure of secondary infection with American genotype dengue 2 to cause dengue haemorrhagic fever. Lancet 354:1431–1434PubMedGoogle Scholar
  95. Weaver SC (1995) Evolution of alphaviruses. In: Gibbs AJ, Calisher CH, Garcia-Arenal F (eds) Molecular basis of virus evolution. Cambridge University Press, Cambridge, pp 501–530Google Scholar
  96. Weaver SC, Barrett AD (2004) Transmission cycles, host range, evolution and emergence of arboviral disease. Nat Rev Microbiol 2:789–801CrossRefPubMedGoogle Scholar
  97. Weaver SC, Scott TW, Lorenz LH (1990) Patterns of eastern equine encephalomyelitis virus infection in Culiseta melanura (Diptera: Culicidae). JMed Entomol 27:878–891Google Scholar
  98. Weaver SC, Rico-Hesse R, Scott TW (1992) Genetic diversity and slow rates of evolution in New World alphaviruses. Curr Topics Microbiol Immunol 176:99–117Google Scholar
  99. Weaver SC, Bellew LA, Gousset L, Repik PM, Scott TW, Holland JJ (1993) Diversity within natural populations of eastern equine encephalomyelitis virus. Virology 195:700–709CrossRefPubMedGoogle Scholar
  100. Weaver SC, Kang W, Shirako Y, Rumenapf T, Strauss EG, Strauss JH (1997) Recombinational history and molecular evolution of western equine encephalomyelitis complex alphaviruses. J Virol 71:613–623PubMedGoogle Scholar
  101. Weaver SC, Brault AC, Kang W, Holland JJ (1999) Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J Virol 73:4316–4326PubMedGoogle Scholar
  102. Weaver SC, Dalgarno L, Frey TK, Huang HV, Kinney RM, Rice CM, Roehrig JT, Shope RE, Strauss EG (2000) Family Togaviridae. In: van Regenmortel MHV, Fauquet CM, Bishop DHL, Carstens EB, Estes MK, Lemon SM, Maniloff J, Mayo MA, McGeogh DJ, Pringle CR, Wickner RB (eds) Virus taxonomy. Classification and nomenclature of viruses. Seventh report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, pp 879–889Google Scholar
  103. Weaver SC, Anishchenko M, Bowen R, Brault AC, Estrada-Franco JG, Fernandez Z, Greene I, Ortiz D, Paessler S, Powers AM (2004a) Genetic determinants of Venezuelan equine encephalitis emergence. Arch Virol Suppl:43–64Google Scholar
  104. Weaver SC, Ferro C, Barrera R, Boshell J, Navarro JC (2004b) Venezuelan equine encephalitis. Annu Rev Entomol 49:141–174CrossRefPubMedGoogle Scholar
  105. Woodall J (2001) Chikungunya virus. In: Service MW (ed) The encyclopedia of arthropod-transmitted infections. CAB International, Wallingford, UK, pp 115–119Google Scholar
  106. Zanotto PM, Gao GF, Gritsun T, Marin MS, Jiang WR, Venugopal K, Reid HW, Gould EA (1995) An arbovirus cline across the northern hemisphere. Virology 210:152–159PubMedGoogle Scholar
  107. Zanotto PM, Gould EA, Gao GF, Harvey PH, Holmes EC (1996) Population dynamics of flaviviruses revealed by molecular phylogenies. Proc Natl Acad Sci U S A 93:548–553CrossRefPubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2006

Authors and Affiliations

  • S. C. Weaver
    • 1
  1. 1.Center for Biodefense and Emerging Infectious Diseases and Department of PathologyUniversity of Texas Medical BranchGalvestonUSA

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