West Nile Virus Experimental Evolution and the Trade-off Hypothesis

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In nature, arthropod-borne viruses (arboviruses) perpetuate through alternating replication in vertebrate and invertebrate hosts. The trade-off hypothesis proposes that these viruses maintain adequate replicative fitness in two disparate hosts in exchange for superior fitness in one host. Releasing the virus from the constraints of a two-host cycle should thus facilitate adaptation to a single host. This theory has been addressed in a variety of systems, but remains poorly understood. We sought to determine the fitness implications of alternating host replication for West Nile virus (WNV) using an in vivo model system. Previously, WNV was serially or alternately passed 20 times in vivo in chicks or mosquitoes and resulting viruses were characterized genetically. In this study, these test viruses were competed in vivo in fitness assays against an unpassed marked reference virus. Fitness was assayed in chicks and in two important WNV vectors, Culex pipiens and Culex quinquefasciatus. Chick-specialized virus displayed clear fitness gains in chicks and in Cx. pipiens but not in Cx. quinquefasciatus. Cx. pipiens-specialized virus experienced reduced fitness in chicks and little change in either mosquito species. These data suggest that when fitness is measured in birds the trade-off hypothesis is supported; but in mosquitoes it is not. Overall, these results suggest that WNV evolution is driven by alternate cycles of genetic expansion in mosquitoes, where purifying selection is weak and genetic diversity generated, and restriction in birds, where purifying selection is strong.

Vyšlo v časopise: West Nile Virus Experimental Evolution and the Trade-off Hypothesis. PLoS Pathog 7(11): e32767. doi:10.1371/journal.ppat.1002335
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002335

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Zdroje

1. EbelGDCarricaburuJYoungDBernardKAKramerLD 2004 Genetic and phenotypic variation of West Nile virus in New York, 2000–2003. Am J Trop Med Hyg 71 493 500

2. DavisCTEbelGDLanciottiRSBraultACGuzmanH 2005 Phylogenetic analysis of North American West Nile virus isolates, 2001–2004: evidence for the emergence of a dominant genotype. Virology 342 252 265

3. SnapinnKWHolmesECYoungDSBernardKAKramerLD 2007 Declining growth rate of West Nile virus in North America. J Virol 81 2531 2534

4. SteinhauerDAHollandJJ 1987 Rapid evolution of RNA viruses. Annu Rev Microbiol 41 409 433

5. JenkinsGMRambautAPybusOGHolmesEC 2002 Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J Mol Evol 54 156 165

6. CiotaATKramerLD 2010 Insights into Arbovirus Evolution and Adaptation from Experimental Studies. Viruses 2 2594 2617

7. WeaverSCBraultACKangWHollandJJ 1999 Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J Virol 73 4316 4326

8. GreeneIPWangEDeardorffERMilleronRDomingoE 2005 Effect of alternating passage on adaptation of sindbis virus to vertebrate and invertebrate cells. J Virol 79 14253 14260

9. CoffeyLLVasilakisNBraultACPowersAMTripetF 2008 Arbovirus evolution in vivo is constrained by host alternation. Proc Natl Acad Sci USA 105 6970 6975

10. VasilakisNDeardorffERKenneyJLRossiSLHanleyKA 2009 Mosquitoes put the brake on arbovirus evolution: experimental evolution reveals slower mutation accumulation in mosquito than vertebrate cells. PLoS Pathog 5 e1000467

11. ChenW-JWuH-RChiouS-S 2003 E/NS1 Modifications of Dengue 2 Virus after Serial Passages in Mammalian and/or Mosquito Cells. Intervirology 46 289 295

12. CiotaATLovelaceAONgoKALeANMaffeiJG 2007 Cell-specific adaptation of two flaviviruses following serial passage in mosquito cell culture. Virology 357 165 174

13. CiotaATJiaYPayneAFJerzakGVSDavisLJ 2009 Experimental passage of St. Louis encephalitis virus in vivo in mosquitoes and chickens reveals evolutionarily significant virus characteristics. PLoS ONE 4 e7876

14. CiotaATLovelaceAOJiaYDavisLJYoungDS 2008 Characterization of mosquito-adapted West Nile virus. J Gen Virol 89 1633 1642

15. BrackneyDEBeaneJEEbelGD 2009 RNAi targeting of West Nile virus in mosquito midguts promotes virus diversification. PLoS Pathog 5 e1000502

16. JerzakGVSBernardKAKramerLDEbelGD 2005 Genetic variation in West Nile virus from naturally infected mosquitoes and birds suggests quasispecies structure and strong purifying selection. J Gen Virol 86 2175 2183

17. JerzakGVSBernardKKramerLDShiP-YEbelGD 2007 The West Nile virus mutant spectrum is host-dependant and a determinant of mortality in mice. Virology 360 469 476

18. JerzakGVSBrownIShiP-YKramerLDEbelGD 2008 Genetic diversity and purifying selection in West Nile virus populations are maintained during host switching. Virology 374 256 260

19. CoffeyLLVignuzziM 2011 Host alternation of chikungunya virus increases fitness while restricting population diversity and adaptability to novel selective pressures. J Virol 85 1025 1035

20. CiotaATLovelaceAOJonesSAPayneAKramerLD 2007 Adaptation of two flaviviruses results in differences in genetic heterogeneity and virus adaptability. J Gen Virol 88 2398 2406

21. FitzpatrickKADeardorffERPeskoKBrackneyDEZhangB 2010 Population variation of West Nile virus confers a host-specific fitness benefit in mosquitoes. Virology 404 89 95

22. TurellMJDohmDJSardelisMROguinnMLAndreadisTG 2005 An update on the potential of north American mosquitoes (Diptera: Culicidae) to transmit West Nile Virus. J Med Entomol 42 57 62

23. MoudyRMMeolaMAMorinL-LLEbelGDKramerLD 2007 A newly emergent genotype of West Nile virus is transmitted earlier and more efficiently by Culex mosquitoes. Am J Trop Med Hyg 77 365 370

24. VanlandinghamDLMcGeeCEKlinglerKAGalbraithSEBarrettADT 2008 Short report: comparison of oral infectious dose of West Nile virus isolates representing three distinct genotypes in Culex quinquefasciatus. Am J Trop Med Hyg 79 951 954

25. HardyJLHoukEJKramerLDReevesWC 1983 Intrinsic factors affecting vector competence of mosquitoes for arboviruses. Annu Rev Entomol 28 229 262

26. BrackneyDEPeskoKBrownIDeardorffERKawatachiJ 2011 West Nile virus genetic diversity is maintained during transmission by Culex pipiens quinquefasciatus mosquitoes. PLoS ONE 6 e24466

27. de la TorreJCHollandJJ 1990 RNA virus quasispecies populations can suppress vastly superior mutant progeny. J Virol 64 6278 6281

28. ShendureJJiH 2008 Next-generation DNA sequencing. Nat Biotechnol 26 1135 1145

29. ShiP-YTilgnerMLoMKKentKABernardKA 2002 Infectious cDNA clone of the epidemic west nile virus from New York City. J Virol 76 5847 5856

30. LoMKTilgnerMBernardKAShiP-Y 2003 Functional analysis of mosquito-borne flavivirus conserved sequence elements within 3′ untranslated region of West Nile virus by use of a reporting replicon that differentiates between viral translation and RNA replication. J Virol 77 10004 10014

31. HallGSLittleDP 2007 Relative quantitation of virus population size in mixed genotype infections using sequencing chromatograms. J Virol Methods 146 22 28