1932

Abstract

For virus infections of multicellular hosts, narrow genetic bottlenecks during transmission and within-host spread appear to be widespread. These bottlenecks will affect the maintenance of genetic variation in a virus population and the prevalence of mixed-strain infections, thereby ultimately determining the strength with which different random forces act during evolution. Here we consider different approaches for estimating bottleneck sizes and weigh their merits. We then review quantitative estimates of bottleneck size during cellular infection, within-host spread, horizontal transmission, and finally vertical transmission. In most cases we find that bottlenecks do regularly occur, although in many cases they appear to be virion-concentration dependent. Finally, we consider the evolutionary implications of genetic bottlenecks during virus infection. Although on average strong bottlenecks will lead to declines in fitness, we consider a number of scenarios in which bottlenecks could also be advantageous for viruses.

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2015-11-09
2024-04-26
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Literature Cited

  1. 1. Chin. SARS Mol. Epidemiol. Consort 2004. Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China. Science 303:1666–69 [Google Scholar]
  2. Gire SK, Goba A, Andersen KG, Sealfon RSG, Park DJ. 2.  et al. 2014. Genomic surveillance elucidates Ebola virus origin and transmission during the 2014 outbreak. Science 345:1369–72 [Google Scholar]
  3. Dieu BTM, Marks H, Siebenga JJ, Goldbach RW, Zuidema D. 3.  et al. 2004. Molecular epidemiology of white spot syndrome virus within Vietnam. J. Gen. Virol. 85:3607–18 [Google Scholar]
  4. Elena SF, Sanjuán R. 4.  2007. Virus evolution: insights from an experimental approach. Annu. Rev. Ecol. Evol. Syst. 38:27–52 [Google Scholar]
  5. Zwart MP, Hemerik L, Cory JS, de Visser JAGM, Bianchi FJ. 5.  et al. 2009. An experimental test of the independent action hypothesis in virus-insect pathosystems. Proc. R. Soc. B 276:2233–42 [Google Scholar]
  6. Bedoya LC, Martínez F, Orzáez D, Daròs JA. 6.  2012. Visual tracking of plant virus infection and movement using a reporter MYB transcription factor that activates anthocyanin biosynthesis. Plant Physiol. 158:1130–38 [Google Scholar]
  7. Bald J. 7.  1937. The use of numbers of infections for comparing the concentration of plant virus suspensions. I. Dilution experiments with purified suspensions. Ann. Appl. Biol. 24:33–55 [Google Scholar]
  8. Smith IR, Crook NE. 8.  1988. In vivo isolation of baculovirus genotypes. Virology 166:240–44 [Google Scholar]
  9. Teunis PFM, Havelaar AH. 9.  2000. The Beta Poisson dose-response model is not a single-hit model. Risk Anal. 20:513–20 [Google Scholar]
  10. Hall JS, French R, Hein GL, Morris TJ, Stenger DC. 10.  2001. Three distinct mechanisms facilitate genetic isolation of sympatric wheat streak mosaic virus lineages. Virology 282:230–36 [Google Scholar]
  11. Sacristán S, Malpica JM, Fraile A, García-Arenal F. 11.  2003. Estimation of population bottlenecks during systemic movement of Tobacco mosaic virus in tobacco plants. J. Virol. 77:9906–11 [Google Scholar]
  12. Li H, Roossinck MJ. 12.  2004. Genetic bottlenecks reduce population variation in an experimental RNA virus population. J. Virol. 78:10582–87 [Google Scholar]
  13. Ali A, Roossinck MJ. 13.  2010. Genetic bottlenecks during systemic movement of Cucumber mosaic virus vary in different host plants. Virology 404:279–83 [Google Scholar]
  14. Teunis PF, Moe CL, Liu P, Miller SE, Lindesmith L. 14.  et al. 2008. Norwalk virus: How infectious is it?. J. Med. Virol. 80:1468–76 [Google Scholar]
  15. Smith DR, Adams AP, Kenney JL, Wang E, Weaver SC. 15.  2008. Venezuelan equine encephalitis virus in the mosquito vector Aedes taeniorhynchus: infection initiated by a small number of susceptible epithelial cells and a population bottleneck. Virology 372:176–86 [Google Scholar]
  16. Zwart MP, Daròs JA, Elena SF. 16.  2011. One is enough: In vivo effective population size is dose-dependent for a plant RNA virus. PLOS Pathog. 7:e1002122 [Google Scholar]
  17. Forrester NL, Guerbois M, Seymour RL, Spratt H, Weaver SC. 17.  2012. Vector-borne transmission imposes a severe bottleneck on an RNA virus population. PLOS Pathog. 8:e1002897 [Google Scholar]
  18. Fabré F, Moury B, Johansen EI, Simon V, Jacquemond M, Senoussi R. 18.  2014. Narrow bottlenecks affect Pea seedborne mosaic virus populations during vertical seed transmission but not during leaf colonization. PLOS Pathog. 10:e1003833 [Google Scholar]
  19. Moury B, Fabré F, Senoussi R. 19.  2007. Estimation of the number of virus particles transmitted by an insect vector. PNAS 104:17891–96 [Google Scholar]
  20. Moya A, Elena SF, Bracho A, Miralles R, Barrio E. 20.  2000. The evolution of RNA viruses: a population genetics view. PNAS 97:6967–73 [Google Scholar]
  21. Simón O, Williams T, Caballero P, López-Ferber M. 21.  2006. Dynamics of deletion genotypes in an experimental insect virus population. Proc. R. Soc. B 273:783–90 [Google Scholar]
  22. Gómez P, Sempere RN, Elena SF, Aranda MA. 22.  2009. Mixed infections of Pepino mosaic virus strains modulate the evolutionary dynamics of this emergent virus. J. Virol. 83:12378–87 [Google Scholar]
  23. Froissart R, Roze D, Uzest M, Galibert L, Blanc S, Michalakis Y. 23.  2005. Recombination every day: abundant recombination in a virus during a single multi-cellular host infection. PLOS Biol. 3:e89 [Google Scholar]
  24. Wright S. 24.  1931. Evolution in Mendelian populations. Genetics 16:97–159 [Google Scholar]
  25. Folimonova SY, Robertson CJ, Shilts T, Folimonov AS, Hilf ME. 25.  et al. 2010. Infection with strains of Citrus tristeza virus does not exclude superinfection by other strains of the virus. J. Virol. 84:1314–25 [Google Scholar]
  26. Kell AM, Wargo AR, Kurath G. 26.  2013. The role of virulence in in vivo superinfection fitness of the vertebrate RNA virus infectious hematopoietic necrosis virus. J. Virol. 87:8145–57 [Google Scholar]
  27. Bergua M, Zwart MP, El-Mohtar C, Shilts T, Elena SF, Folimonova SY. 27.  2014. A viral protein mediates superinfection exclusion at the whole-organism level but is not required for exclusion at the cellular level. J. Virol. 88:11327–38 [Google Scholar]
  28. Dolja VV, McBride HJ, Carrington JC. 28.  1992. Tagging of plant potyvirus replication and movement by insertion of β-glucuronidase into the viral polyprotein. PNAS 89:10208–12 [Google Scholar]
  29. Regoes RR, Hottinger JW, Sygnarski L, Ebert D. 29.  2003. The infection rate of Daphnia magna by Pasteuria ramosa conforms with the mass-action principle. Epidemiol. Infect. 131:957–66 [Google Scholar]
  30. Druett HA. 30.  1952. Bacterial invasion. Nature 170:288 [Google Scholar]
  31. Ridout MJ, Fenlon JS, Hughes PR. 31.  1993. A generalized one-hit model for bioassays of insect viruses. Biometrics 49:1136–41 [Google Scholar]
  32. Ben-Ami F, Regoes RR, Ebert D. 32.  2008. A quantitative test of the relationship between parasite dose and infection probability across different host-parasite combinations. Proc. R. Soc. B 275:853–59 [Google Scholar]
  33. Van der Werf W, Hemerik L, Vlak JM, Zwart MP. 33.  2011. Heterogeneous host susceptibility enhances prevalence of mixed-genotype micro-parasite infections. PLOS Comput. Biol. 7:e1002097 [Google Scholar]
  34. Lafforgue G, Tromas N, Elena SF, Zwart MP. 34.  2012. Dynamics of the establishment of systemic potyvirus infection: independent yet cumulative action of primary infection sites. J. Virol. 86:12912–22 [Google Scholar]
  35. Sánchez-Navarro JA, Zwart MP, Elena SF. 35.  2013. Effects of the number of genome segments on primary and systemic infections with a multipartite plant RNA virus. J. Virol. 87:10805–15 [Google Scholar]
  36. French R, Stenger DC. 36.  2003. Evolution of Wheat streak mosaic virus: dynamics of population growth within plants may explain limited variation. Annu. Rev. Phytopathol. 41:199–214 [Google Scholar]
  37. Meynell GG, Stocker BAD. 37.  1957. Some hypotheses on the aetiology of fatal infections in partially resistant hosts and their application to mice challenged with Salmonella paratyphi-b or Salmonella typhimurium by intraperitoneal injection. J. Gen. Microbiol. 16:38–58 [Google Scholar]
  38. Moxon ER, Murphy PA. 38.  1978. Haemophilus influenzae bacteremia and meningitis resulting from survival of a single organism. PNAS 75:1534–36 [Google Scholar]
  39. Wright S. 39.  1951. The genetical structure of populations. Ann. Eugen. 15:323–54 [Google Scholar]
  40. Weir BS, Cockerham CC. 40.  1984. Estimating F-statistics for the analysis of population structure. Evolution 38:1358–70 [Google Scholar]
  41. Monsion B, Froissart R, Michalakis Y, Blanc S. 41.  2008. Large bottleneck size in Cauliflower mosaic virus populations during host plant colonization. PLOS Pathog. 4:e1000174 [Google Scholar]
  42. Kleczkowski A. 42.  1950. Interpreting relationships between the concentrations of plant viruses and number of local lesions. J. Gen. Microbiol. 4:53–69 [Google Scholar]
  43. Furumoto WA, Mickey R. 43.  1967. A mathematical model for infectivity-dilution curve of tobacco mosaic virus: experimental tests. Virology 32:224–33 [Google Scholar]
  44. Zwart MP, Elena SF. 44.  2015. Testing the independent action hypothesis of plant pathogen mode of action: a simple and powerful new approach. Phytopathology 105:18–25 [Google Scholar]
  45. Miyashita S, Kishino H. 45.  2010. Estimation of the size of genetic bottlenecks in cell-to-cell movement of Soil-borne wheat mosaic virus and the possible role of the bottlenecks in speeding up selection of variations in trans-acting genes or elements. J. Virol. 84:1828–37 [Google Scholar]
  46. Dieu BTM, Zwart MP, Vlak JM. 46.  2010. Can VNTRs be used to study genetic variation within white spot syndrome virus isolates?. J. Fish Dis. 33:689–93 [Google Scholar]
  47. Ercolani GL. 47.  1973. Two hypotheses on the aetiology response of plants to phytopathogenic bacteria. J. Gen. Microbiol. 74:83–95 [Google Scholar]
  48. González-Jara P, Fraile A, Cantó T, García-Arenal F. 48.  2009. The multiplicity of infection of a plant virus varies during colonization of its eukaryotic host. J. Virol. 83:7487–94 [Google Scholar]
  49. Gutiérrez S, Yvon M, Thébaud G, Monsion B, Michalakis Y, Blanc S. 49.  2010. Dynamics of the multiplicity of cellular infection in a plant virus. PLOS Pathog. 6:e1001113 [Google Scholar]
  50. Bull JC, Godfray HC, O'Reilly DR. 50.  2001. Persistence of an occlusion-negative recombinant nucleopolyhedrovirus in Trichoplusia ni indicates high multiplicity of cellular infection. Appl. Environ. Microbiol. 67:5204–9 [Google Scholar]
  51. Bull JC, Godfray HCJ, O'Reilly DR. 51.  2003. A few-polyhedra mutant and wild-type nucleopolyhedrovirus remain as a stable polymorphism during serial coinfection in Trichoplusia ni. Appl. Environ. Microbiol. 69:2052–57 [Google Scholar]
  52. Zwart MP, Tromas N, Elena SF. 52.  2013. Model-selection-based approach for calculating cellular multiplicity of infection during virus colonization of multi-cellular hosts. PLOS ONE 8:e64657 [Google Scholar]
  53. Clavijo G, Williams T, Muñoz D, Caballero P, López-Ferber M. 53.  2010. Mixed genotype transmission bodies and virions contribute to the maintenance of diversity in an insect virus. Proc. R. Soc. B 277:943–51 [Google Scholar]
  54. Tromas N, Zwart MP, Lafforgue G, Elena SF. 54.  2014. Within-host spatiotemporal dynamics of plant virus infection at the cellular level. PLOS Genet. 10:e1004186 [Google Scholar]
  55. González-Jara P, Fraile A, Cantó T, Garcia-Arenal F. 55.  2013. Author's correction: The multiplicity of infection of a plant virus varies during colonization of its eukaryotic host. J. Virol. 87:2374 [Google Scholar]
  56. Iranzo J, Manrubia SC. 56.  2012. Evolutionary dynamics of genome segmentation in multipartite viruses. Proc. R. Soc. B 279:3812–19 [Google Scholar]
  57. Jridi C, Martin JF, Marie-Jeanne V, Labonne G, Blanc S. 57.  2006. Distinct viral populations differentiate and evolve independently in a single perennial host plant. J. Virol. 80:2349–57 [Google Scholar]
  58. Gutiérrez S, Yvon M, Pirolles E, Garzo E, Fereres A. 58.  et al. 2012. Circulating virus load determines the size of bottlenecks in viral populations progressing within a host. PLOS Pathog. 8:e1003009 [Google Scholar]
  59. Forrester NL, Coffey LL, Weaver SC. 59.  2014. Arboviral bottlenecks and challenges to maintaining diversity and fitness during mosquito transmission. Viruses 6:3991–4004 [Google Scholar]
  60. Brackney DE, Pesko KN, Brown IK, Deardorff ER, Kawatachi J, Ebel GD. 60.  2011. West Nile virus genetic diversity is maintained during transmission by Culex pipiens quinquefasciatus mosquitoes. PLOS ONE 6:e24466 [Google Scholar]
  61. Kuss SK, Etheredge CA, Pfeiffer JK. 61.  2008. Multiple host barriers restrict poliovirus trafficking in mice. PLOS Pathog. 4:e1000082 [Google Scholar]
  62. Gorman S, Harvey NL, Moro D, Lloyd ML, Voigt V. 62.  et al. 2006. Mixed infection with multiple strains of murine cytomegalovirus occurs following simultaneous or sequential infection of immunocompetent mice. J. Gen. Virol. 87:1123–32 [Google Scholar]
  63. Kirkwood TB, Bangham CR. 63.  1994. Cycles, chaos, and evolution in virus cultures: a model of defective interfering particles. PNAS 91:8685–89 [Google Scholar]
  64. Zwart MP, Pijlman GP, Sardanyés J, Duarte J, Januário C, Elena SF. 64.  2013. Complex dynamics of defective interfering baculoviruses during serial passage in insect cells. J. Biol. Phys. 39:327–42 [Google Scholar]
  65. Bull RA, Luciani F, McElroy K, Gaudieri S, Pham ST. 65.  et al. 2011. Sequential bottlenecks drive viral evolution in early acute hepatitis C virus infection. PLOS Pathog. 7:e1002243 [Google Scholar]
  66. Betancourt M, Fereres A, Fraile A, García-Arenal F. 66.  2008. Estimation of the effective number of founders that initiate an infection after aphid transmission of a multipartite plant virus. J. Virol. 82:12416–21 [Google Scholar]
  67. Sacristán S, Díaz M, Fraile A, García-Arenal F. 67.  2011. Contact transmission of Tobacco mosaic virus: a quantitative analysis of parameters relevant for virus evolution. J. Virol. 85:4974–81 [Google Scholar]
  68. Stewart AD, Logsdon JM Jr, Kelley SE. 68.  2005. An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution 59:730–39 [Google Scholar]
  69. Pagán I, Montes N, Milgroom MG, García-Arenal F. 69.  2014. Vertical transmission selects for reduced virulence in a plant virus and for increased resistance in the host. PLOS Pathog. 10:e1004293 [Google Scholar]
  70. Elena SF, Sanjuán R, Bordería AV, Turner PE. 70.  2001. Transmission bottlenecks and the evolution of fitness in rapidly evolving RNA viruses. Infect. Genet. Evol. 1:41–48 [Google Scholar]
  71. Russell ES, Kwiek JJ, Keys J, Barton K, Mwapasa V. 71.  et al. 2011. The genetic bottleneck in vertical transmission of subtype C HIV-1 is not driven by selection of especially neutralization-resistant virus from the maternal viral population. J. Virol. 85:8253–62 [Google Scholar]
  72. Chao L. 72.  1990. Fitness of RNA virus decreased by Muller's ratchet. Nature 348:454–55 [Google Scholar]
  73. Duarte EA, Clarke DK, Moya A, Domingo E, Holland JJ. 73.  1992. Rapid fitness losses in mammalian RNA virus clones due to Muller's ratchet. PNAS 89:6015–19 [Google Scholar]
  74. Yuste E, Sánchez-Palomino S, Casado C, Domingo E, López-Galíndez C. 74.  1999. Drastic fitness loss in human immunodeficiency virus type 1 upon serial bottleneck events. J. Virol. 73:2745–51 [Google Scholar]
  75. Lazaro E, Escarmís C, Pérez-Mercader J, Manrubia SC, Domingo E. 75.  2003. Resistance of virus to extinction on bottleneck passages: study of a decaying and fluctuating pattern of fitness loss. PNAS 100:10830–35 [Google Scholar]
  76. de la Iglesia F, Elena SF. 76.  2007. Fitness declines in Tobacco etch virus upon serial bottleneck transfers. J. Virol. 81:4941–47 [Google Scholar]
  77. Jaramillo N, Domingo E, Muñoz-Egea MC, Tabarés E, Gadea I. 77.  2013. Evidence of Muller's ratchet in herpes simplex virus type 1. J. Gen. Virol. 94:366–75 [Google Scholar]
  78. Lynch M, Conery JS, Bürger R. 78.  1995. Mutation accumulation and the extinction of small populations. Am. Nat. 146:489–518 [Google Scholar]
  79. Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R. 79.  2006. Quasispecies diversity determines pathogenesis through cooperative interactions within a viral population. Nature 439:344–48 [Google Scholar]
  80. Coffey LL, Beeharry Y, Bordería AV, Blanc H, Vignuzzi M. 80.  2011. Arbovirus high fidelity variant loses fitness in mosquitoes and mice. PNAS 108:16038–43 [Google Scholar]
  81. Zwart MP, Willemsen A, Daròs JA, Elena SF. 81.  2014. Experimental evolution of pseudogenization and gene loss in a plant RNA virus. Mol. Biol. Evol. 31:121–34 [Google Scholar]
  82. Zwart MP, Erro E, van Oers MM, de Visser JAGM, Vlak JM. 82.  2008. Low multiplicity of infection in vivo results in purifying selection against baculovirus deletion mutants. J. Gen. Virol. 89:1220–24 [Google Scholar]
  83. Wright S. 83.  1932. The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proc. Int. Congr. Genet., 6th, Ithaca, N.Y. DF Jones 356–66 Menasha, WI: Brooklyn Bot. Garden [Google Scholar]
  84. Elena SF, Solé RV, Sardanyés J. 84.  2010. Simple genomes, complex interactions: epistasis in RNA virus. Chaos 20:026106 [Google Scholar]
  85. Lalić J, Elena SF. 85.  2012. Magnitude and sign epistasis among deleterious mutations in a positive-sense plant RNA virus. Heredity 109:71–77 [Google Scholar]
  86. Da Silva J, Wyatt SK. 86.  2014. Fitness valleys constrain HIV-1's adaptation to its secondary chemokine coreceptor. J. Evol. Biol. 27:604–15 [Google Scholar]
  87. Poelwijk FJ, Tănase-Nicola S, Kiviet DJ, Tans SJ. 87.  2011. Reciprocal sign epistasis is a necessary condition for multi-peaked fitness landscapes. J. Theor. Biol. 272:141–44 [Google Scholar]
  88. Burch CL, Chao L. 88.  2000. Evolvability of an RNA virus is determined by its mutational neighbourhood. Nature 406:625–28 [Google Scholar]
  89. Sanjuán R, Cuevas JM, Furio V, Holmes EC, Moya A. 89.  2007. Selection for robustness in mutagenized RNA viruses. PLOS Genet. 3:e93 [Google Scholar]
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