Evolutionary influences in arboviral disease

Current Topics in Microbiology and Immunology

Volumn 299, Issue , 2006, Pages 285-314

  Weaver, S C ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AEDES AEGYPTI; AFRICAN SWINE FEVER VIRUS; ALPHA VIRUS; ARBOVIRUS; BUNYAVIRUS; CULEX PIPIENS; DENGUE VIRUS; DNA VIRUS; EVOLUTIONARY ADAPTATION; EVOLUTIONARY RATE; FLAVIVIRUS; GENETIC REASSORTMENT; GENETIC STABILITY; GENUS; HOST; NEIGHBOR JOINING METHOD; NONHUMAN; ORTHOMYXOVIRUS; PARASITE VECTOR; PARSIMONY ANALYSIS; PHENOTYPE; PHYLOGENETIC TREE; PRIORITY JOURNAL; REOVIRUS; REVIEW; RHABDOVIRUS; RNA VIRUS; TAXONOMY; TOGAVIRUS; VIRUS RECOMBINATION; VIRUS TRANSMISSION; WESTERN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ARBOVIRUS INFECTIONS; ARBOVIRUSES; EVOLUTION, MOLECULAR; FLAVIVIRUS; HUMANS; PHYLOGENY; REASSORTANT VIRUSES; RECOMBINATION, GENETIC;

AEDES AEGYPTI; AFRICAN SWINE FEVER VIRUS; ALPHAVIRUS; ARBOVIRUS; ARTHROPODA; BUNYAVIRIDAE; CULEX PIPIENS; DENGUE VIRUS; DNA VIRUSES; FLAVIVIRIDAE; FLAVIVIRUS; ORTHOBUNYAVIRUS; ORTHOMYXOVIRIDAE; REOVIRIDAE; REOVIRUS SP.; RHABDOVIRIDAE; RNA VIRUSES; TOGAVIRIDAE; VERTEBRATA; WESTERN EQUINE ENCEPHALOMYELITIS VIRUS;

EID: 30644459759     PISSN: 0070217X     EISSN: None     Source Type: Book Series    
DOI: 10.1007/3-540-26397-7_10     Document Type: Review

References (107)

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 68:539-544
2. Baldridge GD, Beaty BJ, Hewlett MJ (1989) Genomic stability of La Crosse virus during vertical and horizontal transmission. Arch Virol 108:89-99
3. Baric RS, Yount B, Hensley L, Peel SA, Chen W (1997) Episodic evolution mediates interspecies transfer of a murine coronavirus. J Virol 71:1946-1955
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 309:190-195
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 20:1650-1658
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 11:87-94
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 75:8298-8305
8. Borucki MK, Chandler LJ, Parker BM, Blair CD, Beaty BJ (1999) Bunyavirus superinfection and segment reassortment in transovarially infected mosquitoes. J Gen Virol 80:3173-3179
9. Bouloy M (2001) Rift Valley fever virus. In: Service MW (ed) The Encyclopedia of arthropod-transmitted Infections. CAB International, Wallingford, UK, pp 426-434
10. Brault AC (2001) Genetic analysis of epizootic venezuelan equine encephalitis virus emergence mechanisms. In: Pathology. University of Texas Medical Branch, Galveston, Texas, p 318
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 61:579-586
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 76:1718-1730
13. Brault AC, Powers AM, Weaver SC (2002b) Vector infection determinants of Venezuelan equine encephalitis virus reside within the E2 envelope glycoprotein. J Virol 76:6387-6392
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 101:11344-11349
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 9:926-933
16. Byrnes AP, Griffin DE (1998) Binding of Sindbis virus to cell surface heparan sulfate. J Virol 72:7349-7356
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 19-57
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 60:286-291
19. Cilnis MJ, Kang W, Weaver SC (1996) Genetic conservation of Highlands J viruses. Virology 218:343-351
20. Collins WE (1963) Transmission of Semliki Forest virus by Anopheles albimanus using membrane feeding techniques. Mosq News 23:96-99
21. Cooper LA, Scott TW (2001) Differential evolution of eastern equine encephalitis virus populations in response to host cell type. Genetics 157:1403-1412
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 77:4463-4467
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 85:1971-1980
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 9:362-367
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 89:6015-6019
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 70:3355-3362
27. Endy TP, Nisalak A (2002) Japanese encephalitis virus: ecology and epidemiology. Curr Top Microbiol Immunol 267:11-48
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 96:790-794
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 78:8922-8926
30. Gould EA, de Lamballerie X, Zanotto PM, Holmes EC (2003) Origins, evolution, and vector/host coadaptations within the genus Flavivirus. Adv Virus Res 59:277-314
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 79:9128-9133
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)
33. Griffin DE (2001) Alphaviruses. In: Knipe DM, Howley PM (eds) Fields' virology, 4th edn. Lippincott, Williams and Wilkins, New York, pp 917-962
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 25:146-150
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 85:5997-6001
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 38:411-422
37. Hertz JM, Huang HV (1992) Utilization of heterologous alphavirus junction sequences as promoters by Sindbis virus. J Virol 66:857-864
38. Hertz JM, Huang HV (1995a) Evolution of the Sindbis virus subgenomic mRNA promoter in cultured cells. J Virol 69:7768-7774
39. Hertz JM, Huang HV (1995b) Host-dependent evolution of the Sindbis virus promoter for subgenomic mRNA synthesis. J Virol 69:7775-7781
40. Hilgard P, Stockert R (2000) Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes. Hepatology 32:1069-1077
41. Holland J, Domingo E (1998) Origin and evolution of viruses. Virus Genes 16:13-21
42. Holland JJ, Spindler K, Horodyski F, Grabau E, Nichol S, VandePol S (1982) Rapid evolution of RNA genomes. Science 215:1577-1585
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 65:2960-2967
44. Holmes EC (2003) Molecular clocks and the puzzle of RNA virus origins. J Virol 77:3893-3897
45. Holmes EC, Twiddy SS (2003) The origin, emergence and evolutionary genetics of dengue virus. Infect Genet Evol 3:19-28
46. Hughes AL (2001) Evolutionary change of predicted cytotoxic T cell epitopes of dengue virus. Infect Genet Evol 1:123-130
47. Hurlbut HS (1966) Mosquito salivation and virus transmission. Am J Trop Med Hyg 15:989-993
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 11:172-176
49. Karabatsos N (1985) International catalogue of arboviruses. Am Soc Trop Med Hyg, San Antonio
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.
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 72:7357-7366
52. Kramer LD, Chandler LJ (2001) Phylogenetic analysis of the envelope gene of St. Louis encephalitis virus. Arch Virol 146:2341-2355
53. Lamotte LC Jr (1960) Japanese B encephalitis virus in the organs of infected mosquitoes. Am J Hyg 72:73-87
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 78:12717-12721
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, pp 991-1041
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 89:65-73
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 165:245-255
58. Lopez S, Yao JS, Kuhn RJ, Strauss EG, Strauss JH (1994) Nucleocapsid-glycoprotein interactions required for assembly of alphaviruses. J Virol 68:1316-1323
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 11:225-237
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 38:813-821
61. Moncayo AC, Fernandez Z, Diallo M, Ortiz D, Sail A, Hartman S, Davis CT, Coffey LL, Mathiot CC, Tesh RB, Weaver SC (2004) Dengue emergence and adaptation to peridomestic mosquitoes. Emerg Infect Dis 10:1790-1796
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 72:57-64
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 41:575-581
64. Norder H, Lundstrom JO, Kozuch O, Magnius LO (1996) Genetic relatedness of Sindbis virus strains from Europe, Middle East, and Africa. Virology 222:440-445
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 69:6805-6809
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 287:459-465
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 41:987-993
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 Barman Forest virus. Am J Trop Med Hyg 57:230-234
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 81:471-479
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 75:10118-10131
71. Ross RW (1955) A laboratory technique for studying the insect transmission of animal viruses, employing a bat-wing membrane, demonstrated with two African viruses. In: Annual Report, Virus Research Institute, Entebbe, Uganda, pp 192-200
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 7
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 85:2289-2297
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 212:20-29
75. Sammels LM, Lindsay MD, Poidinger M, Coelen RJ, Mackenzie JS (1999) Geographic distribution and evolution of Sindbis virus in Australia. J Gen Virol 80:739-748
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, pp 895-916
77. Scott TW, Weaver SC (1989) Eastern equine encephalomyelitis virus: epidemiology and evolution of mosquito transmission. Adv Virus Res 37:277-328
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 180:411-415
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 10:1337-1351
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 73:33-39
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 77:3091-3098
82. Strauss JH, Strauss EG (1994) The alphaviruses: gene expression, replication, and evolution. Microbiol Rev 58:491-562
83. Tabachnick WJ, Powell JR (1979) A world-wide survey of genetic variation in the yellow fever mosquito, Aedes aegypti. Genet Res 34:215-229
84. Taylor WP, Marshall ID (1975a) Adaptation studies with Ross River virus: laboratory mice and cell cultures. J Gen Virol 28:59-72
85. Taylor WP, Marshall ID (1975b) Adaptation studies with Ross River virus: retention of field level virulence. J Gen Virol 28:73-83
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 10:593-597
87. Tsai TF, Weaver SC, Monath TP (2002) Alphaviruses. In: Richman DD, Whitley RJ, Hayden FG (eds) Clinical virology. ASM Press, Washington, DC, pp 1177-1210
88. Turell MJ, Sardelis MR, O'Guinn ML, Dohm DJ (2002) Potential vectors of West Nile virus in North America. Curr Top Microbiol Immunol 267:241-252
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 298:63-72
90. Twiddy SS, Woelk CH, Holmes EC (2002b) Phylogenetic evidence for adaptive evolution of dengue viruses in nature. J Gen Virol 83:1679-1689
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 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 71:120-123
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 74:3227-3234
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 354:1431-1434
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 501-530
96. Weaver SC, Barrett AD (2004) Transmission cycles, host range, evolution and emergence of arboviral disease. Nat Rev Microbiol 2:789-801
97. Weaver SC, Scott TW, Lorenz LH (1990) Patterns of eastern equine encephalomyelitis virus infection in Culiseta melanura (Diptera: Culicidae). J Med Entomol 27:878-891
98. Weaver SC, Rico-Hesse R, Scott TW (1992) Genetic diversity and slow rates of evolution in New World alphaviruses. Curr Topics Microbiol Immunol 176:99-117
99. Weaver SC, Bellew LA, Gousset L, Repik PM, Scott TW, Holland JJ (1993) Diversity within natural populations of eastern equine encephalomyelitis virus. Virology 195:700-709
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 71:613-623
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 73:4316-4326
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 879-889
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:43-64
104. Weaver SC, Ferro C, Barrera R, Boshell J, Navarro JC (2004b) Venezuelan equine encephalitis. Annu Rev Entomol 49:141-174
105. Woodall J (2001) Chikungunya virus. In: Service MW (ed) The encyclopedia of arthropod-transmitted infections. CAB International, Wallingford, UK, pp 115-119
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 210:152-159
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 93:548-553