Twenty years of West Nile virus spread and evolution in the Americas visualized by Nextstrain

English version

Autoři: James Hadfield ^aff001; Anderson F. Brito ^aff002; Daniele M. Swetnam ^aff003; Chantal B. F. Vogels ^aff002; Ryan E. Tokarz ^aff004; Kristian G. Andersen ^aff005; Ryan C. Smith ^aff004; Trevor Bedford ^aff001; Nathan D. Grubaugh ^aff002
Působiště autorů: Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America ^aff001; Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, Connecticut, United States of America ^aff002; Department of Pathology, Microbiology and Immunology, University of California, Davis, Davis, California, United States of America ^aff003; Department of Entomology, Iowa State University, Ames, Iowa, United States of America ^aff004; Department of Immunology and Microbiology, Scripps Research, La Jolla, California, United States of America ^aff005; Scripps Research Translational Institute, La Jolla, California, United States of America ^aff006
Vyšlo v časopise: Twenty years of West Nile virus spread and evolution in the Americas visualized by Nextstrain. PLoS Pathog 15(10): e32767. doi:10.1371/journal.ppat.1008042
Kategorie: Review
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1008042

Souhrn

It has been 20 years since West Nile virus first emerged in the Americas, and since then, little progress has been made to control outbreaks caused by this virus. After its first detection in New York in 1999, West Nile virus quickly spread across the continent, causing an epidemic of human disease and massive bird die-offs. Now the virus has become endemic to the United States, where an estimated 7 million human infections have occurred, making it the leading mosquito-borne virus infection and the most common cause of viral encephalitis in the country. To bring new attention to one of the most important mosquito-borne viruses in the Americas, we provide an interactive review using Nextstrain: a visualization tool for real-time tracking of pathogen evolution (nextstrain.org/WNV/NA). Nextstrain utilizes a growing database of more than 2,000 West Nile virus genomes and harnesses the power of phylogenetics for students, educators, public health workers, and researchers to visualize key aspects of virus spread and evolution. Using Nextstrain, we use virus genomics to investigate the emergence of West Nile virus in the U S, followed by its rapid spread, evolution in a new environment, establishment of endemic transmission, and subsequent international spread. For each figure, we include a link to Nextstrain to allow the readers to directly interact with and explore the underlying data in new ways. We also provide a brief online narrative that parallels this review to further explain the data and highlight key epidemiological and evolutionary features (nextstrain.org/narratives/twenty-years-of-WNV). Mirroring the dynamic nature of outbreaks, the Nextstrain links provided within this paper are constantly updated as new West Nile virus genomes are shared publicly, helping to stay current with the research. Overall, our review showcases how genomics can track West Nile virus spread and evolution, as well as potentially uncover novel targeted control measures to help alleviate its public health burden.

Klíčová slova:

Genome analysis – Phylogeography – Birds – Viral genomics – Viral evolution – West Nile virus – Mosquitoes – Bird genomics

Zdroje

1. Kramer LD, Styer LM, Ebel GD. A global perspective on the epidemiology of West Nile virus. Annu Rev Entomol. 2008;53: 61–81. doi: 10.1146/annurev.ento.53.103106.093258 17645411

2. Komar N. West Nile virus: epidemiology and ecology in North America. Adv Virus Res. 2003;61: 185–234. 14714433

3. Reisen WK. Ecology of West Nile virus in North America. Viruses. 2013;5: 2079–2105. doi: 10.3390/v5092079 24008376

4. CDC. West Nile Virus Final Cumulative Maps and Data [Internet]. 10 Dec 2018. Available from: https://www.cdc.gov/westnile/statsmaps/finalmapsdata/index.html. [cited 2019 May 5].

5. Ronca SE, Murray KO, Nolan MS. Cumulative incidence of West Nile virus infection, continental United States, 1999–2016. Emerg Infect Dis. 2019;25: 325. doi: 10.3201/eid2502.180765 30666940

6. CDC. 8 Zoonotic Diseases Shared Between Animals and People of Most Concern in the U.S [Internet]. 6 May 2019. Available from: https://www.cdc.gov/media/releases/2019/s0506-zoonotic-diseases-shared.html. [cited 2019 May 13].

7. Aphis U. West Nile Virus Maps- States with Equine Cases [Internet]. Available from: https://www.aphis.usda.gov/aphis/ourfocus/animalhealth/animal-disease-information/horse-disease-information/wnv/west-nile-virus. [cited 2019 Jan 25].

8. George TL, Harrigan RJ, LaManna JA, DeSante DF, Saracco JF, Smith TB. Persistent impacts of West Nile virus on North American bird populations. Proc Natl Acad Sci U S A. 2015;112: 14290–14294. doi: 10.1073/pnas.1507747112 26578774

9. LaDeau SL, Kilpatrick AM, Marra PP. West Nile virus emergence and large-scale declines of North American bird populations. Nature. 2007;447: 710–713. doi: 10.1038/nature05829 17507930

10. Public Health Agency of Canada. Surveillance of West Nile virus [Internet]. 26 Jun 2015. Available from: https://www.canada.ca/en/public-health/services/diseases/west-nile-virus/surveillance-west-nile-virus.html. [cited 2019 May 26].

11. Castro-Jorge LA de, Siconelli MJL, Ribeiro BDS, Moraes FM de, Moraes JB de, Agostinho MR, et al. West Nile virus infections are here! Are we prepared to face another flavivirus epidemic? Rev Soc Bras Med Trop. 2019;52: e20190089. doi: 10.1590/0037-8682-0089-2018 30942263

12. Elizondo-Quiroga D, Elizondo-Quiroga A. West nile virus and its theories, a big puzzle in Mexico and Latin America. J Glob Infect Dis. 2013;5: 168–175. doi: 10.4103/0974-777X.122014 24672180

13. Who P. West nile virus Epidemiological alerts and updates [Internet]. Available from: https://www.paho.org/hq/index.php?option=com_topics&view=rdmore&cid=2195&Itemid=40782&lang=en. [cited 2019 May 26].

14. Grubaugh ND, Ladner JT, Lemey P, Pybus OG, Rambaut A, Holmes EC, et al. Tracking virus outbreaks in the twenty-first century. Nat Microbiol. 2019;4: 10–19. doi: 10.1038/s41564-018-0296-2 30546099

15. Volz EM, Koelle K, Bedford T. Viral phylodynamics. PLoS Comput Biol. 2013;9: e1002947. doi: 10.1371/journal.pcbi.1002947 23555203

16. Grubaugh ND, Ladner JT, Kraemer MUG, Dudas G, Tan AL, Gangavarapu K, et al. Genomic epidemiology reveals multiple introductions of Zika virus into the United States. Nature. 2017;90: 4864.

17. Metsky HC, Matranga CB, Wohl S, Schaffner SF, Freije CA, Winnicki SM, et al. Zika virus evolution and spread in the Americas. Nature. 2017;66: 366.

18. Faria NR, Quick J, Claro IM, Thézé J, de Jesus JG, Giovanetti M, et al. Establishment and cryptic transmission of Zika virus in Brazil and the Americas. Nature. 2017; doi: 10.1038/nature22401 28538727

19. Faria NR, Kraemer MUG, Hill SC, Goes de Jesus J, Aguiar RS, Iani FCM, et al. Genomic and epidemiological monitoring of yellow fever virus transmission potential. Science. 2018; doi: 10.1126/science.aat7115 30139911

20. Moreira-Soto A, Torres MC, Lima de Mendonça MC, Mares-Guia MA, Dos Santos Rodrigues CD, Fabri AA, et al. Evidence for multiple sylvatic transmission cycles during the 2016–2017 yellow fever virus outbreak, Brazil. Clin Microbiol Infect. 2018;24: 1019.e1–1019.e4.

21. Lanciotti RS, Roehrig JT, Deubel V, Smith J, Parker M, Steele K, et al. Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science. 1999;286: 2333–2337. doi: 10.1126/science.286.5448.2333 10600742

22. Hepp CM, Cocking JH, Valentine M, Young SJ, Damian D, Samuels-Crow KE, et al. Phylogenetic analysis of West Nile Virus in Maricopa county, Arizona: Evidence for dynamic behavior of strains in two major lineages in the American Southwest. PLoS ONE. 2018;13: e0205801. doi: 10.1371/journal.pone.0205801 30475820

23. Duggal NK, Reisen WK, Fang Y, Newman RM, Yang X, Ebel GD, et al. Genotype-specific variation in West Nile virus dispersal in California. Virology. 2015;485: 79–85. doi: 10.1016/j.virol.2015.07.004 26210076

24. Di Giallonardo F, Geoghegan JL, Docherty DE, McLean RG, Zody MC, Qu J, et al. Fluid spatial dynamics of West Nile virus in the United States: Rapid spread in a permissive host environment. J Virol. 2016;90: 862–872. doi: 10.1128/JVI.02305-15 26512086

25. Davis CT, Ebel GD, Lanciotti RS, Brault AC, Guzman H, Siirin M, et al. Phylogenetic analysis of North American West Nile virus isolates, 2001–2004: Evidence for the emergence of a dominant genotype. Virology. 2005;342: 252–265. doi: 10.1016/j.virol.2005.07.022 16137736

26. Pybus OG, Suchard MA, Lemey P, Bernardin FJ, Rambaut A, Crawford FW, et al. Unifying the spatial epidemiology and molecular evolution of emerging epidemics. Proc Natl Acad Sci U S A. 2012;109: 15066–15071. doi: 10.1073/pnas.1206598109 22927414

27. Swetnam D, Widen SG, Wood TG, Reyna M, Wilkerson L, Debboun M, et al. Terrestrial bird migration and West Nile virus circulation, United States. Emerg Infect Dis. 2018;24: 2184–2194. doi: 10.3201/eid2412.180382 30457531

28. Ladner JT, Grubaugh ND, Pybus OG, Andersen KG. Precision epidemiology for infectious disease control. Nat Med. 2019;25: 206–211. doi: 10.1038/s41591-019-0345-2 30728537

29. Dellicour S, Baele G, Dudas G, Faria NR, Pybus OG, Suchard MA, et al. Phylodynamic assessment of intervention strategies for the West African Ebola virus outbreak. Nat Commun. 2018;9: 2222. doi: 10.1038/s41467-018-03763-2 29884821

30. Hadfield J, Megill C, Bell SM, Huddleston J, Potter B, Callender C, et al. Nextstrain: Real-time tracking of pathogen evolution. Bioinformatics. 2018;34: 4121–4123. doi: 10.1093/bioinformatics/bty407 29790939

31. GISAID. Global Initiative on Sharing All Influenza Data [Internet]. Available from: https://www.gisaid.org/. [cited 2019 May 18].

32. Neher RA, Bedford T. Nextflu: Real-time tracking of seasonal influenza virus evolution in humans. Bioinformatics. 2015;31: 3546–3548. doi: 10.1093/bioinformatics/btv381 26115986

33. Neher RA, Bedford T, Daniels RS, Russell CA, Shraiman BI. Prediction, dynamics, and visualization of antigenic phenotypes of seasonal influenza viruses. Proc Natl Acad Sci U S A. 2016;113: E1701–9. doi: 10.1073/pnas.1525578113 26951657

34. Gardy JL, Loman NJ. Towards a genomics-informed, real-time, global pathogen surveillance system. Nat Rev Genet. 2018;19: 9–20. doi: 10.1038/nrg.2017.88 29129921

35. Sagulenko P, Puller V, Neher RA. TreeTime: Maximum-likelihood phylodynamic analysis. Virus Evol. 2018;4: vex042. doi: 10.1093/ve/vex042 29340210

36. Briese T, Jia XY, Huang C, Grady LJ, Lipkin WI. Identification of a Kunjin/West Nile-like flavivirus in brains of patients with New York encephalitis. Lancet. 1999;354: 1261–1262. doi: 10.1016/s0140-6736(99)04576-6 10520637

37. CDC. Outbreak of West Nile-like viral encephalitis—New York, 1999. MMWR Morb Mortal Wkly Rep. 1999;48: 845–849. 10563521

38. Exotic diseases close to home. Lancet. 1999;354: 1221. 10520624

39. Jia XY, Briese T, Jordan I, Rambaut A, Chi HC, Mackenzie JS, et al. Genetic analysis of West Nile New York 1999 encephalitis virus. Lancet. 1999;354: 1971–1972. doi: 10.1016/s0140-6736(99)05384-2 10622305

40. Smithburn KC, Hughes TP, Burke AW, Paul JH. A neurotropic virus isolated from the blood of a native of Uganda. Am J Trop Med Hyg. 1940;s1-20: 471–492.

41. Mackenzie JS, Gubler DJ, Petersen LR. Emerging flaviviruses: The spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat Med. 2004;10: S98–109. doi: 10.1038/nm1144 15577938

42. May FJ, Davis CT, Tesh RB, Barrett ADT. Phylogeography of West Nile virus: From the cradle of evolution in Africa to Eurasia, Australia, and the Americas. J Virol. 2011;85: 2964–2974. doi: 10.1128/JVI.01963-10 21159871

43. Zehender G, Ebranati E, Bernini F, Lo Presti A, Rezza G, Delogu M, et al. Phylogeography and epidemiological history of West Nile virus genotype 1a in Europe and the Mediterranean basin. Infection, Genetics and Evolution. 2011;11: 646–653. doi: 10.1016/j.meegid.2011.02.003 21320643

44. Johnston BL, Conly JM. West Nile virus—where did it come from and where might it go? Canadian Journal of Infectious Diseases. 2000;11: 175–178. doi: 10.1155/2000/856598 18159286

45. Tian H, Sun Z, Faria NR, Yang J, Cazelles B, Huang S, et al. Increasing airline travel may facilitate co-circulation of multiple dengue virus serotypes in Asia. PLoS Negl Trop Dis. 2017;11: e0005694. doi: 10.1371/journal.pntd.0005694 28771468

46. Viana DS, Santamaría L, Figuerola J. Migratory birds as global dispersal vectors. Trends Ecol Evol. 2016;31: 763–775. doi: 10.1016/j.tree.2016.07.005 27507683

47. Hernández-Triana LM, Jeffries CL, Mansfield KL, Carnell G, Fooks AR, Johnson N. Emergence of West Nile virus lineage 2 in Europe: A review on the introduction and spread of a mosquito-borne disease. Front Public Health. 2014;2: 271. doi: 10.3389/fpubh.2014.00271 25538937

48. Reed KD, Meece JK, Henkel JS, Shukla SK. Birds, migration and emerging zoonoses: West Nile virus, Lyme disease, influenza A and enteropathogens. Clin Med Res. 2003;1: 5–12. 15931279

49. CDC. West Nile Virus Activity—United States, September 26-October 2, 2002, and Investigations of West Nile Virus Infections in Recipients of Blood Transfusion and Organ Transplantation [Internet]. 23 Oct 2002. Available from: https://www.cdc.gov/mmwr/preview/mmwrhtml/mm5139a5.htm. [cited 2019 May 5].

50. Reisen W, Lothrop H, Chiles R, Madon M, Cossen C, Woods L, et al. West Nile virus in California. Emerg Infect Dis. 2004;10: 1369–1378. doi: 10.3201/eid1008.040077 15496236

51. Beasley DWC, Davis CT, Guzman H, Vanlandingham DL, Travassos da Rosa APA, Parsons RE, et al. 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 12758166

52. Herring BL, Bernardin F, Caglioti S, Stramer S, Tobler L, Andrews W, et al. Phylogenetic analysis of WNV in North American blood donors during the 2003–2004 epidemic seasons. Virology. 2007;363: 220–228. doi: 10.1016/j.virol.2007.01.019 17321561

53. Grinev A, Chancey C, Volkova E, Añez G, Heisey DAR, Winkelman V, et al. Genetic variability of West Nile virus in US blood donors from the 2012 epidemic season. PLoS Negl Trop Dis. 2016;10: e0004717. doi: 10.1371/journal.pntd.0004717 27182734

54. Anez G, Grinev A, Chancey C, Ball C, Akolkar N, Land KJ, et al. Evolutionary dynamics of West Nile virus in the United States, 1999–2011: Phylogeny, selection pressure and evolutionary time-scale analysis. PLoS Negl Trop Dis. 2013;7: e2245. doi: 10.1371/journal.pntd.0002245 23738027

55. Davis CT, Beasley DWC, Guzman H, Raj R, D’Anton M, Novak RJ, et al. Genetic variation among temporally and geographically distinct West Nile virus isolates, United States, 2001, 2002. Emerg Infect Dis. 2003;9: 1423–1429. doi: 10.3201/eid0911.030301 14718086

56. Bertolotti L, Kitron UD, Walker ED, Ruiz MO, Brawn JD, Loss SR, et al. Fine-scale genetic variation and evolution of West Nile Virus in a transmission “hot spot” in suburban Chicago, USA. Virology. 2008;374: 381–389. doi: 10.1016/j.virol.2007.12.040 18261758

57. Amore G, Bertolotti L, Hamer GL, Kitron UD, Walker ED, Ruiz MO, et al. Multi-year evolutionary dynamics of West Nile virus in suburban Chicago, USA, 2005–2007. Philos Trans R Soc Lond B Biol Sci. 2010;365: 1871–1878. doi: 10.1098/rstb.2010.0054 20478882

58. Bertolotti L, Kitron U, Goldberg TL. Diversity and evolution of West Nile virus in Illinois and the United States, 2002–2005. Virology. 2007;360: 143–149. doi: 10.1016/j.virol.2006.10.030 17113619

59. Komar N, Langevin S, Hinten S, Nemeth N, Edwards E, Hettler D, et al. Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerg Infect Dis. 2003;9: 311–322. doi: 10.3201/eid0903.020628 12643825

60. Turell MJ, O’Guinn M, Oliver J. Potential for New York mosquitoes to transmit West Nile virus. Am J Trop Med Hyg. 2000;62: 413–414. doi: 10.4269/ajtmh.2000.62.413 11037788

61. Goddard LB, Roth AE, Reisen WK, Scott TW. Vector competence of California mosquitoes for West Nile virus. Emerg Infect Dis. 2002;8: 1385–1391. doi: 10.3201/eid0812.020536 12498652

62. Sardelis MR, Turell MJ, Dohm DJ, O’Guinn ML. Vector competence of selected North American Culex and Coquillettidia mosquitoes for West Nile virus. Emerg Infect Dis. 2001;7: 1018–1022. doi: 10.3201/eid0706.010617 11747732

63. Rappole JH, Compton BW, Leimgruber P, Robertson J, King DI, Renner SC. Modeling movement of West Nile virus in the western hemisphere. Vector Borne Zoonotic Dis. 2006;6: 128–139. doi: 10.1089/vbz.2006.6.128 16796510

64. Venkatesan M, Rasgon JL. Population genetic data suggest a role for mosquito-mediated dispersal of West Nile virus across the western United States. Mol Ecol. 2010;19: 1573–1584. doi: 10.1111/j.1365-294X.2010.04577.x 20298466

65. Owen J, Moore F, Panella N, Edwards E, Bru R, Hughes M, et al. Migrating birds as dispersal vehicles for West Nile virus. Ecohealth. 2006;3: 79.

66. Dusek RJ, McLean RG, Kramer LD, Ubico SR, Dupuis AP 2nd, Ebel GD, et al. Prevalence of West Nile virus in migratory birds during spring and fall migration. Am J Trop Med Hyg. 2009;81: 1151–1158. doi: 10.4269/ajtmh.2009.09-0106 19996451

67. Reisen WK, Wheeler SS, Garcia S, Fang Y. Migratory birds and the dispersal of arboviruses in California. Am J Trop Med Hyg. 2010;83: 808–815. doi: 10.4269/ajtmh.2010.10-0200 20889869

68. Rappole JH, Derrickson SR, Hubálek Z. Migratory birds and spread of West Nile virus in the western hemisphere. Emerg Infect Dis. 2000;6: 319–328. doi: 10.3201/eid0604.000401 10905964

69. Weaver SC, Rico-Hesse R, Scott TW. Genetic diversity and slow rates of evolution in New World alphaviruses. Current Topics in Microbiology and Immunology. 1992; 99–117. doi: 10.1007/978-3-642-77011-1_7 1318187

70. Weaver SC, Brault AC, Kang W, Holland JJ. Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J Virol. 1999;73: 4316–4326. 10196330

71. Ciota AT, Lovelace AO, Ngo KA, Le AN, Maffei JG, Franke MA, et al. Cell-specific adaptation of two flaviviruses following serial passage in mosquito cell culture. Virology. 2007;357: 165–174. doi: 10.1016/j.virol.2006.08.005 16963095

72. Grubaugh ND, Fauver JR, Ruckert C, Weger-Lucarelli J, Garcia-Luna S, Murrieta RA, et al. Mosquitoes transmit unique West Nile virus populations during each feeding episode. Cell Rep. 2017;19: 709–718. doi: 10.1016/j.celrep.2017.03.076 28445723

73. Deardorff ER, Fitzpatrick KA, Jerzak GVS, Shi P-Y, Kramer LD, Ebel GD. West Nile virus experimental evolution in vivo and the trade-off hypothesis. PLoS Pathog. 2011;7: e1002335. doi: 10.1371/journal.ppat.1002335 22102808

74. Jenkins GM, Rambaut A, Pybus OG, Holmes EC. Rates of molecular evolution in RNA viruses: A quantitative phylogenetic analysis. J Mol Evol. 2002;54: 156–165. doi: 10.1007/s00239-001-0064-3 11821909

75. Granwehr BP, Li L, Davis CT, Beasley DWC, Barrett ADT. Characterization of a West Nile virus isolate from a human on the Gulf Coast of Texas. J Clin Microbiol. 2004;42: 5375–5377. doi: 10.1128/JCM.42.11.5375-5377.2004 15528747

76. Ebel GD, Carricaburu J, Young D, Bernard KA, Kramer LD. Genetic and phenotypic variation of West Nile virus in New York, 2000–2003. Am J Trop Med Hyg. 2004;71: 493–500. 15516648

77. Moudy RM, Meola MA, Morin L-LL, Ebel GD, Kramer LD. A newly emergent genotype of West Nile virus is transmitted earlier and more efficiently by Culex mosquitoes. Am J Trop Med Hyg. 2007;77: 365–370. 17690414

78. Kilpatrick AM, Meola MA, Moudy RM, Kramer LD. Temperature, viral genetics, and the transmission of West Nile virus by Culex pipiens mosquitoes. PLoS Pathog. 2008;4: e1000092. doi: 10.1371/journal.ppat.1000092 18584026

79. Duggal NK, Bosco-Lauth A, Bowen RA, Wheeler SS, Reisen WK, Felix TA, et al. Evidence for co-evolution of West Nile virus and house sparrows in North America. PLoS Negl Trop Dis. 2014;8: e3262. doi: 10.1371/journal.pntd.0003262 25357248

80. Anderson JF, Main AJ, Cheng G, Ferrandino FJ, Fikrig E. Horizontal and vertical transmission of West Nile virus genotype NY99 by Culex salinarius and genotypes NY99 and WN02 by Culex tarsalis. Am J Trop Med Hyg. 2012;86: 134–139. doi: 10.4269/ajtmh.2012.11-0473 22232464

81. Vanlandingham DL, McGee CE, Klingler KA, Galbraith SE, Barrett ADT, Higgs S. Short report: Comparison of oral infectious dose of West Nile virus isolates representing three distinct genotypes in Culex quinquefasciatus. Am J Trop Med Hyg. 2008;79: 951–954. 19052310

82. Danforth ME, Reisen WK, Barker CM. Extrinsic incubation rate is not accelerated in recent California strains of West Nile virus in Culex tarsalis (Diptera: Culicidae). J Med Entomol. 2015;52: 1083–1089. doi: 10.1093/jme/tjv082 26336222

83. Grubaugh ND, Smith DR, Brackney DE, Bosco-Lauth AM, Fauver JR, Campbell CL, et al. Experimental evolution of an RNA virus in wild birds: Evidence for host-dependent impacts on population structure and competitive fitness. PLoS Pathog. 2015;11: e1004874. doi: 10.1371/journal.ppat.1004874 25993022

84. Grubaugh ND, Weger-Lucarelli J, Murrieta RA, Fauver JR, Garcia-Luna SM, Prasad AN, et al. Genetic drift during systemic arbovirus infection of mosquito vectors leads to decreased relative fitness during host switching. Cell Host Microbe. 2016;19: 481–492. doi: 10.1016/j.chom.2016.03.002 27049584

85. McMullen AR, May FJ, Li L, Guzman H, Bueno R Jr, Dennett JA, et al. Evolution of new genotype of West Nile virus in North America. Emerg Infect Dis. 2011;17: 785–793. doi: 10.3201/eid1705.101707 21529385

86. Añez G, Grinev A, Chancey C, Ball C, Akolkar N, Land KJ, et al. Evolutionary dynamics of West Nile virus in the United States, 1999–2011: Phylogeny, selection pressure and evolutionary time-scale analysis. PLoS Negl Trop Dis. 2013;7: e2245. doi: 10.1371/journal.pntd.0002245 23738027

87. Bialosuknia SM, Tan Y, Zink SD, Koetzner CA, Maffei JG, Halpin RA, et al. Evolutionary dynamics and molecular epidemiology of West Nile virus in New York State: 1999–2015. Virus Evol. 2019;5: vez020. doi: 10.1093/ve/vez020 31341640

88. Paull SH, Horton DE, Ashfaq M, Rastogi D, Kramer LD, Diffenbaugh NS, et al. Drought and immunity determine the intensity of West Nile virus epidemics and climate change impacts. Proceedings of the Royal Society B. 2017; doi: 10.1098/rspb.2016.2078 28179512

89. Landesman WJ, Allan BF, Langerhans RB, Knight TM, Chase JM. Inter-annual associations between precipitation and human incidence of West Nile virus in the United States. Vector Borne Zoonotic Dis. 2007;7. doi: 10.1089/vbz.2006.0590 17867908

90. Shaman J, Day JF, Stieglitz M. Drought-induced amplification and epidemic transmission of West Nile virus in southern Florida. J Med Entomol. 2005;42: 134–141. doi: 10.1093/jmedent/42.2.134 15799522

91. Wimberly MC, Lamsal A, Giacomo P, Chuang TW. Regional variation of climatic influences on West Nile virus outbreaks in the United States. Am J Trop Med Hyg. 2014;91: 677–684. doi: 10.4269/ajtmh.14-0239 25092814

92. Ruiz MO, Chaves LF, Hamer GL, Sun T, Brown WM, Walker ED, et al. Local impact of temperature and precipitation on West Nile virus infection in Culex species mosquitoes in northeast Illinois, USA. Parasit Vectors. 2010;3: 19. doi: 10.1186/1756-3305-3-19 20302617

93. Davis JK, Vincent G, Hildreth MB, Kightlinger L, Carlson C, Wimberly MC. Integrating environmental monitoring and mosquito surveillance to predict vector-borne disease: Prospective forecasts of a West Nile virus outbreak. PLoS Curr. 2017; doi: 10.1371/currents.outbreaks.90e80717c4e67e1a830f17feeaaf85de 28736681

94. Chuang TW, Wimberly MC. Remote sensing of climatic anomalies and West Nile virus incidence in the northern great plains of the United States. PLoS ONE. 2012;7: 1–10.

95. Ciota AT, Kramer LD. Vector-virus interactions and transmission dynamics of West Nile virus. Viruses. 2013;5: 3021–3047. doi: 10.3390/v5123021 24351794

96. Kilpatrick AM. Globalization, land use, and the invasion of West Nile virus. Science. 2011;334: 323–327. doi: 10.1126/science.1201010 22021850

97. Dunphy BM, Kovach KB, Gehrke EJ, Field EN, Rowley WA, Bartholomay LC, et al. Long-term surveillance defines spatial and temporal patterns implicating Culex tarsalis as the primary vector of West Nile virus. Sci Rep. 2019;9: 6637. doi: 10.1038/s41598-019-43246-y 31036953

98. Andreadis TG. The contribution of Culex pipiens complex mosquitoes to transmission and persistence of West Nile virus in North America. Journal of American Mosquito Control Association. 2012;28: 137–151.

99. Gibbs SEJ, Wimberly MC, Madden M, Masour J, Yabsley MJ, Stallknecht DE. Factors affecting the geographic distribution of West Nile virus in Georgia, USA: 2002–2004. Vector Borne Zoonotic Dis. 2006;6: 73–82. doi: 10.1089/vbz.2006.6.73 16584329

100. Bowden SE, Magori K, Drake JM. Regional differences in the association between land cover and West Nile virus disease incidence in humans in the United States. Am J Trop Med Hyg. 2011;84: 234–238. doi: 10.4269/ajtmh.2011.10-0134 21292890

101. Kothera L, Godsey MS, Doyle MS, Savage HM. Characterization of Culex pipiens complex (Diptera: Culicidae) populations in Colorado, USA using microsatellites. PLoS ONE. 2012;7: 1–9.

102. Ciota AT, Chin PA, Kramer LD. The effect of hybridization of Culex pipiens complex mosquitoes on transmission of West Nile virus. Parasit Vectors. 2013;6: 305. doi: 10.1186/1756-3305-6-305 24499581

103. Giordano BV, Kaur S, Hunter FF. West Nile virus in Ontario, Canada: A twelve-year analysis of human case prevalence, mosquito surveillance, and climate data. PLoS ONE. 2017;12: e0183568. doi: 10.1371/journal.pone.0183568 28829827

104. Dupuis AP 2nd, Marra PP, Kramer LD. Serologic evidence of West Nile virus transmission, Jamaica, West Indies. Emerg Infect Dis. 2003;9: 860–863. doi: 10.3201/eid0907.030249 12890329

105. Estrada-Franco JG, Navarro-Lopez R, Beasley DW, Coffey L, Carrara AS, da Rosa A T, et al. West Nile virus in Mexico: Evidence of widespread circulation since July 2002. Emerging Infectious Diseases. 2003;9. doi: 10.3201/eid0912.030564 14720402

106. Komar N, Clark GG. West Nile virus activity in Latin America and the Caribbean. Revista Panamericana de Salud Pública. 2006;19: 112–117. doi: 10.1590/s1020-49892006000200006 16551385

107. Elizondo-Quiroga D, Davis CT, Fernandez-Salas I, Escobar-Lopez R, Velasco Olmos D, Soto Gastalum LC, et al. West Nile Virus isolation in human and mosquitoes, Mexico. Emerg Infect Dis. 2005;11: 1449–1452. doi: 10.3201/eid1109.050121 16229779

108. Mattar S, Edwards E, Laguado J, González M, Alvarez J, Komar N. West Nile virus antibodies in Colombian horses. Emerg Infect Dis. 2005;11: 1497–1498. doi: 10.3201/eid1109.050426 16673523

109. Morales MA, Barrandeguy M, Fabbri C, Garcia JB, Vissani A, Trono K, et al. West Nile virus isolation from equines in Argentina, 2006. Emerg Infect Dis. 2006;12: 1559–1561. doi: 10.3201/eid1210.060852 17176571

110. Bosch I, Herrera F, Navarro J-C, Lentino M, Dupuis A, Maffei J, et al. West Nile virus, Venezuela. Emerg Infect Dis. 2007;13: 651–653. doi: 10.3201/eid1304.061383 17561567

111. Pauvolid-Corrêa A, Morales MA, Levis S, Figueiredo LTM, Couto-Lima D, Campos Z, et al. Neutralising antibodies for West Nile virus in horses from Brazilian Pantanal. Mem Inst Oswaldo Cruz. 2011;106: 467–474. doi: 10.1590/s0074-02762011000400014 21739036

112. Ulloa A, Ferguson HH, Méndez-Sánchez JD, Danis-Lozano R, Casas-Martínez M, Bond JG, et al. West Nile virus activity in mosquitoes and domestic animals in Chiapas, México. Vector Borne Zoonotic Dis. 2009;9: 555–560. doi: 10.1089/vbz.2008.0087 19281433

113. Dudas G, Bedford T. The ability of single genes vs full genomes to resolve time and space in outbreak analysis [Internet]. bioRxiv. 2019. p. 582957. doi: 10.1101/582957

114. Mann BR, McMullen AR, Guzman H, Tesh RB, Barrett ADT. Dynamic transmission of West Nile virus across the United States-Mexican border. Virology. 2013;436: 75–80. doi: 10.1016/j.virol.2012.10.023 23141421

115. Deardorff E, Estrada-Franco J, Brault AC, Navarro-Lopez R, Campomanes-Cortes A, Paz-Ramirez P, et al. Introductions of West Nile virus strains to Mexico. Emerg Infect Dis. 2006;12: 314–318. doi: 10.3201/eid1202.050871 16494762

116. Osorio JE, Ciuoderis KA, Lopera JG, Piedrahita LD, Murphy D, Levasseur J, et al. Characterization of West Nile viruses isolated from captive American flamingoes (Phoenicopterus ruber) in Medellin, Colombia. Am J Trop Med Hyg. 2012;87: 565–572. doi: 10.4269/ajtmh.2012.11-0655 22802436

117. Fabbri CM, García JB, Morales MA, Enría DA, Levis S, Lanciotti RS. Complete genome sequences and phylogenetic analysis of two West Nile virus strains isolated from equines in Argentina in 2006 could indicate an early introduction of the virus in the Southern Cone. Vector Borne Zoonotic Dis. 2014;14: 794–800. doi: 10.1089/vbz.2014.1588 25409270

118. Martins LC, Silva EVP da, Casseb LMN, Silva SP da, Cruz ACR, Pantoja JA de S, et al. First isolation of West Nile virus in Brazil. Mem Inst Oswaldo Cruz. 2019;114: e180332. doi: 10.1590/0074-02760180332 30672980

119. Anthony SJ, Garner MM, Palminteri L, Navarrete-Macias I, Sanchez-Leon MD, Briese T, et al. West Nile virus in the British Virgin Islands. Ecohealth. 2014;11: 255–257. doi: 10.1007/s10393-014-0910-6 24504904

120. Mann BR, McMullen AR, Swetnam DM, Barrett ADT. Molecular epidemiology and evolution of West Nile virus in North America. Int J Environ Res Public Health. 2013;10: 5111–5129. doi: 10.3390/ijerph10105111 24135819

121. Barrera R, Hunsperger E, Muñoz-Jordán JL, Amador M, Diaz A, Smith J, et al. First isolation of West Nile virus in the Caribbean. Am J Trop Med Hyg. 2008;78: 666–668. 18385366

122. Gubler DJ. The continuing spread of West Nile virus in the western hemisphere. Clin Infect Dis. 2007;45: 1039–1046. doi: 10.1086/521911 17879923

123. Kopp A, Gillespie TR, Hobelsberger D, Estrada A, Harper JM, Miller RA, et al. Provenance and geographic spread of St. Louis encephalitis virus. MBio. 2013;4: e00322–13. doi: 10.1128/mBio.00322-13 23760463

124. Diaz A, Coffey LL, Burkett-Cadena N, Day JF. Reemergence of St. Louis Encephalitis Virus in the Americas. Emerg Infect Dis. 2018;24. doi: 10.3201/eid2412.180372 30457961

125. Quick J, Grubaugh ND, Pullan ST, Claro IM, Smith AD, Gangavarapu K, et al. Multiplex PCR method for MinION and Illumina sequencing of Zika and other virus genomes directly from clinical samples. Nature Protocols. 2017;12: 1261–1276. doi: 10.1038/nprot.2017.066 28538739

126. Metsky HC, Siddle KJ, Gladden-Young A, Qu J, Yang DK, Brehio P, et al. Capturing sequence diversity in metagenomes with comprehensive and scalable probe design. Nat Biotechnol. 2019;37: 160–168. doi: 10.1038/s41587-018-0006-x 30718881

127. Gubler DJ, Campbell GL, Nasci R, Komar N, Petersen L, Roehrig JT. West Nile virus in the United States: Guidelines for detection, prevention, and control. Viral Immunology. 2000;13: 469–475. doi: 10.1089/vim.2000.13.469 11192293

128. Rund SSC, Martinez ME. Rescuing hidden ecological data to tackle emerging mosquito-borne diseases. Available from: https://www.biorxiv.org/content/early/2017/08/09/096875.abstract. 2017; 096875. [cited 2019 June 11].

129. Dudas G, Carvalho LM, Bedford T, Tatem AJ, Baele G, Faria NR, et al. Virus genomes reveal factors that spread and sustained the Ebola epidemic. Nature. 2017;544: 309–315. doi: 10.1038/nature22040 28405027