1932

Abstract

The evolutionary dynamics of a virus can differ within hosts and across populations. Studies of within-host evolution provide an important link between experimental studies of virus evolution and large-scale phylodynamic analyses. They can determine the extent to which global processes are recapitulated on local scales and how accurately experimental infections model natural ones. They may also inform epidemiologic models of disease spread and reveal how host-level dynamics contribute to a virus's evolution at a larger scale. Over the last decade, advances in viral sequencing have enabled detailed studies of viral genetic diversity within hosts. I review how within-host diversity is sampled, measured, and expressed, and how comparative studies of viral diversity can be leveraged to elucidate a virus's evolutionary dynamics. These concepts are illustrated with detailed reviews of recent research on the within-host evolution of influenza virus, dengue virus, and cytomegalovirus.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-010320-061642
2020-09-29
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/virology/7/1/annurev-virology-010320-061642.html?itemId=/content/journals/10.1146/annurev-virology-010320-061642&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Domingo E, Sabo D, Taniguchi T, Weissmann C 1978. Nucleotide sequence heterogeneity of an RNA phage population. Cell 13:735–44
    [Google Scholar]
  2. 2. 
    Parvin JD, Moscona A, Pan WT, Leider JM, Palese P 1986. Measurement of the mutation rates of animal viruses: influenza A virus and poliovirus type 1. J. Virol. 59:2377–83
    [Google Scholar]
  3. 3. 
    Crotty S, Maag D, Arnold JJ, Zhong W, Lau JYN et al. 2000. The broad-spectrum antiviral ribonucleoside ribavirin is an RNA virus mutagen. Nat. Med. 6:121375–79
    [Google Scholar]
  4. 4. 
    Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R 2006. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439:7074344–48
    [Google Scholar]
  5. 5. 
    Aaskov J. 2006. Long-term transmission of defective RNA viruses in humans and Aedes mosquitoes. Science 311:5758236–38
    [Google Scholar]
  6. 6. 
    Ghedin E, Laplante J, DePasse J, Wentworth DE, Santos RP et al. 2011. Deep sequencing reveals mixed infection with 2009 pandemic influenza A (H1N1) virus strains and the emergence of oseltamivir resistance. J. Infect. Dis. 203:2168–74
    [Google Scholar]
  7. 7. 
    Kao RR, Haydon DT, Lycett SJ, Murcia PR 2014. Supersize me: how whole-genome sequencing and big data are transforming epidemiology. Trends Microbiol 22:5282–91
    [Google Scholar]
  8. 8. 
    Houldcroft CJ, Beale MA, Breuer J 2017. Clinical and biological insights from viral genome sequencing. Nat. Rev. Microbiol. 15:3183–92
    [Google Scholar]
  9. 9. 
    Sanjuan R, Nebot MR, Chirico N, Mansky LM, Belshaw R 2010. Viral mutation rates. J. Virol. 84:199733–48
    [Google Scholar]
  10. 10. 
    Peck KM, Lauring AS. 2018. Complexities of viral mutation rates. J. Virol. 92:14e01031
    [Google Scholar]
  11. 11. 
    Renner DW, Szpara ML. 2017. Impacts of genome-wide analyses on our understanding of human herpesvirus diversity and evolution. J. Virol. 92:1e00908
    [Google Scholar]
  12. 12. 
    Samuel CE. 2011. Adenosine deaminases acting on RNA (ADARs) are both antiviral and proviral. Virology 411:2180–93
    [Google Scholar]
  13. 13. 
    Harris RS, Dudley JP. 2015. APOBECs and virus restriction. Virology 479/480 131–45
    [Google Scholar]
  14. 14. 
    Pérez-Losada M, Arenas M, Galán JC, Palero F, González-Candelas F 2015. Recombination in viruses: mechanisms, methods of study, and evolutionary consequences. Infect. Genet. Evol. 30:296–307
    [Google Scholar]
  15. 15. 
    McDonald SM, Nelson MI, Turner PE, Patton JT 2016. Reassortment in segmented RNA viruses: mechanisms and outcomes. Nat. Rev. Microbiol. 14:7448–60
    [Google Scholar]
  16. 16. 
    Rouzine IM, Rodrigo A, Coffin JM 2001. Transition between stochastic evolution and deterministic evolution in the presence of selection: general theory and application to virology. Microbiol. Mol. Biol. Rev. 65:1151–85
    [Google Scholar]
  17. 17. 
    Moya A, Holmes EC, González-Candelas F 2004. The population genetics and evolutionary epidemiology of RNA viruses. Nat. Rev. Microbiol. 2:4279–88
    [Google Scholar]
  18. 18. 
    Frost SDW, Magalis BR, Kosakovsky Pond SL 2018. Neutral theory and rapidly evolving viral pathogens. Mol. Biol. Evol. 35:61348–54
    [Google Scholar]
  19. 19. 
    McCrone JT, Lauring AS. 2018. Genetic bottlenecks in intraspecies virus transmission. Curr. Opin. Virol. 28:20–25
    [Google Scholar]
  20. 20. 
    Kennedy DA, Dwyer G. 2018. Effects of multiple sources of genetic drift on pathogen variation within hosts. PLOS Biol 16:3e2004444
    [Google Scholar]
  21. 21. 
    Metzker ML. 2010. Sequencing technologies—the next generation. Nat. Rev. Genet. 11:131–46
    [Google Scholar]
  22. 22. 
    McWhite CD, Meyer AG, Wilke CO 2016. Sequence amplification via cell passaging creates spurious signals of positive adaptation in influenza virus H3N2 hemagglutinin. Virus Evol 2:2vew026
    [Google Scholar]
  23. 23. 
    Crotty S, Cameron CE, Andino R 2001. RNA virus error catastrophe: direct molecular test by using ribavirin. PNAS 98:126895–900
    [Google Scholar]
  24. 24. 
    Levi LI, Gnädig NF, Beaucourt S, McPherson MJ, Baron B et al. 2010. Fidelity variants of RNA dependent RNA polymerases uncover an indirect, mutagenic activity of amiloride compounds. PLOS Pathog 6:10e1001163
    [Google Scholar]
  25. 25. 
    Thai KTD, Henn MR, Zody MC, Tricou V, Nguyet NM et al. 2012. High-resolution analysis of intrahost genetic diversity in dengue virus serotype 1 infection identifies mixed infections. J. Virol. 86:2835–43
    [Google Scholar]
  26. 26. 
    Beerenwinkel N, Zagordi O. 2011. Ultra-deep sequencing for the analysis of viral populations. Curr. Opin. Virol. 1:5413–18
    [Google Scholar]
  27. 27. 
    Pauly MD, Procario MC, Lauring AS 2017. A novel twelve class fluctuation test reveals higher than expected mutation rates for influenza A viruses. eLife 6:e26437
    [Google Scholar]
  28. 28. 
    Robasky K, Lewis NE, Church GM 2014. The role of replicates for error mitigation in next-generation sequencing. Nat. Rev. Genet. 15:156–62
    [Google Scholar]
  29. 29. 
    McCrone JT, Lauring AS. 2016. Measurements of intrahost viral diversity are extremely sensitive to systematic errors in variant calling. J. Virol. 90:156884–95
    [Google Scholar]
  30. 30. 
    Gallet R, Fabre F, Michalakis Y, Blanc S 2017. The number of target molecules of the amplification step limits accuracy and sensitivity in ultradeep-sequencing viral population studies. J. Virol. 91:16e00561
    [Google Scholar]
  31. 31. 
    Grubaugh ND, Gangavarapu K, Quick J, Matteson NL, De Jesus JG et al. 2019. An amplicon-based sequencing framework for accurately measuring intrahost virus diversity using PrimalSeq and iVar. Genome Biol 20:18
    [Google Scholar]
  32. 32. 
    Illingworth CJR, Roy S, Beale MA, Tutill H, Williams R, Breuer J 2017. On the effective depth of viral sequence data. Virus Evol 3:2vex030
    [Google Scholar]
  33. 33. 
    Magurran A, McGill B. 2011. Biological Diversity: Frontiers in Measurement and Assessment Oxford, UK: Oxford Univ. Press
  34. 34. 
    Gregori J, Salicrú M, Domingo E, Sanchez A, Esteban JI et al. 2014. Inference with viral quasispecies diversity indices: clonal and NGS approaches. Bioinformatics 30:81104–11
    [Google Scholar]
  35. 35. 
    Zhao L, Illingworth CJR. 2019. Measurements of intrahost viral diversity require an unbiased diversity metric. Virus Evol 5:1vey041
    [Google Scholar]
  36. 36. 
    Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:3585–95
    [Google Scholar]
  37. 37. 
    Nei M, Gojobori T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3:5418–26
    [Google Scholar]
  38. 38. 
    Nelson CW, Hughes AL. 2015. Within-host nucleotide diversity of virus populations: Insights from next-generation sequencing. Infect. Genet. Evol. 30:1–7
    [Google Scholar]
  39. 39. 
    Cuevas JM, Domingo-Calap P, Sanjuán R 2012. The fitness effects of synonymous mutations in DNA and RNA viruses. Mol. Biol. Evol. 29:117–20
    [Google Scholar]
  40. 40. 
    Visher E, Whitefield SE, McCrone JT, Fitzsimmons W, Lauring AS 2016. The mutational robustness of influenza A virus. PLOS Pathog 12:8e1005856
    [Google Scholar]
  41. 41. 
    Kryazhimskiy S, Plotkin JB. 2008. The population genetics of dN/dS. . PLOS Genet 4:12e1000304
    [Google Scholar]
  42. 42. 
    Lin J-J, Bhattacharjee MJ, Yu C-P, Tseng YY, Li W-H 2019. Many human RNA viruses show extraordinarily stringent selective constraints on protein evolution. PNAS 116:3819009–18
    [Google Scholar]
  43. 43. 
    Parameswaran P, Wang C, Trivedi SB, Eswarappa M, Montoya M et al. 2017. Intrahost selection pressures drive rapid dengue virus microevolution in acute human infections. Cell Host Microbe 22:3400–10
    [Google Scholar]
  44. 44. 
    Debbink K, McCrone JT, Petrie JG, Truscon R, Johnson E et al. 2017. Vaccination has minimal impact on the intrahost diversity of H3N2 influenza viruses. PLOS Pathog 13:1e1006194
    [Google Scholar]
  45. 45. 
    Illingworth CJR. 2015. Fitness inference from short-read data: within-host evolution of a reassortant H5N1 influenza virus. Mol. Biol. Evol. 32:113012–26
    [Google Scholar]
  46. 46. 
    Sobel LA, McClain MT, Smith GJD, Wentworth DE, Halpin RA et al. 2016. Deep sequencing of influenza A virus from a human challenge study reveals a selective bottleneck and only limited intrahost genetic diversification. J. Virol. 90:2411247–58
    [Google Scholar]
  47. 47. 
    Imai H, Dinis JM, Zhong G, Moncla LH, Lopes TJS et al. 2018. Diversity of influenza A(H5N1) viruses in infected humans, northern Vietnam, 2004–2010. Emerg. Infect. Dis. 24:71128–238
    [Google Scholar]
  48. 48. 
    Xue KS, Stevens-Ayers T, Campbell AP, Englund JA, Pergam SA et al. 2017. Parallel evolution of influenza across multiple spatiotemporal scales. eLife 6:e26875
    [Google Scholar]
  49. 49. 
    Moncla LH, Bedford T, Dussart P, Horm SV, Rith S et al. 2020. Quantifying within-host evolution of H5N1 influenza in humans and poultry in Cambodia. PLOS Pathog 16:1e1008191
    [Google Scholar]
  50. 50. 
    McCrone JT, Woods RJ, Martin ET, Malosh RE, Monto AS, Lauring AS 2018. Stochastic processes constrain the within and between host evolution of influenza virus. eLife 7:e35962
    [Google Scholar]
  51. 51. 
    Renzette N, Gibson L, Bhattacharjee B, Fisher D, Schleiss MR et al. 2013. Rapid intrahost evolution of human cytomegalovirus is shaped by demography and positive selection. PLOS Genet 9:9e1003735
    [Google Scholar]
  52. 52. 
    Feder AF, Rhee S-Y, Holmes SP, Shafer RW, Petrov DA, Pennings PS 2016. More effective drugs lead to harder selective sweeps in the evolution of drug resistance in HIV-1. eLife 5:e10670
    [Google Scholar]
  53. 53. 
    Foll M, Shim H, Jensen JD 2015. WFABC: a Wright–Fisher ABC-based approach for inferring effective population sizes and selection coefficients from time-sampled data. Mol. Ecol. Resour. 15:187–98
    [Google Scholar]
  54. 54. 
    Kimura M. 1955. Solution of a process of random genetic drift with a continuous model. PNAS 41:144–50
    [Google Scholar]
  55. 55. 
    Williamson EG, Slatkin M. 1999. Using maximum likelihood to estimate population size from temporal changes in allele frequencies. Genetics 152:2755–61
    [Google Scholar]
  56. 56. 
    Kouyos RD, Althaus CL, Bonhoeffer S 2006. Stochastic or deterministic: What is the effective population size of HIV-1?. Trends Microbiol 14:12507–11
    [Google Scholar]
  57. 57. 
    Varble A, Albrecht RA, Backes S, Crumiller M, Bouvier NM et al. 2014. Influenza A virus transmission bottlenecks are defined by infection route and recipient host. Cell Host Microbe 16:5691–700
    [Google Scholar]
  58. 58. 
    Tao H, Steel J, Lowen AC 2014. Intrahost dynamics of influenza virus reassortment. J. Virol. 88:137485–92
    [Google Scholar]
  59. 59. 
    Sobel LA, McClain MT, Smith GJD, Wentworth DE, Halpin RA et al. 2017. The effective rate of influenza reassortment is limited during human infection. PLOS Pathog 13:2e1006203
    [Google Scholar]
  60. 60. 
    Valesano AL, Fitzsimmons WJ, McCrone JT, Petrie JG, Monto AS et al. 2019. Influenza B viruses exhibit lower within-host diversity than influenza A viruses in human hosts. J. Virol. 94:5e01710
    [Google Scholar]
  61. 61. 
    Dinis JM, Florek NW, Fatola OO, Moncla LH, Mutschler JP et al. 2016. Deep sequencing reveals potential antigenic variants at low frequencies in influenza A virus-infected humans. J. Virol. 90:73355–65
    [Google Scholar]
  62. 62. 
    Rambaut A, Pybus OG, Nelson MI, Viboud C, Taubenberger JK, Holmes EC 2008. The genomic and epidemiological dynamics of human influenza A virus. Nature 453:7195615–19
    [Google Scholar]
  63. 63. 
    Bedford T, Suchard MA, Lemey P, Dudas G, Gregory V et al. 2014. Integrating influenza antigenic dynamics with molecular evolution. eLife 3:e01914
    [Google Scholar]
  64. 64. 
    Bedford T, Riley S, Barr IG, Broor S, Chadha M et al. 2015. Global circulation patterns of seasonal influenza viruses vary with antigenic drift. Nature 523:7559217–20
    [Google Scholar]
  65. 65. 
    Pierson TC, Diamond MS. 2013. Flaviviruses. Field's Virology DM Knipe, PM Howley 747–94 Philadelphia: Lippincott Williams & Wilkins, 6th ed..
    [Google Scholar]
  66. 66. 
    Halstead SB. 1988. Pathogenesis of dengue: challenges to molecular biology. Science 239:4839476–81
    [Google Scholar]
  67. 67. 
    Lequime S, Fontaine A, Ar Gouilh M, Moltini-Conclois I, Lambrechts L 2016. Genetic drift, purifying selection and vector genotype shape dengue virus intra-host genetic diversity in mosquitoes. PLOS Genet 12:6e1006111
    [Google Scholar]
  68. 68. 
    Forrester NL, Guerbois M, Seymour RL, Spratt H, Weaver SC 2012. Vector-borne transmission imposes a severe bottleneck on an RNA virus population. PLOS Pathog 8:9e1002897
    [Google Scholar]
  69. 69. 
    Lequime S, Richard V, Cao-Lormeau V-M, Lambrechts L 2017. Full-genome dengue virus sequencing in mosquito saliva shows lack of convergent positive selection during transmission by Aedes aegypti. . Virus Evol 3:2vex031
    [Google Scholar]
  70. 70. 
    Grubaugh ND, Weger-Lucarelli J, Murrieta RA, Fauver JR, Garcia-Luna SM et al. 2016. Genetic drift during systemic arbovirus infection of mosquito vectors leads to decreased relative fitness during host switching. Cell Host Microbe 19:4481–92
    [Google Scholar]
  71. 71. 
    Grubaugh ND, Fauver JR, Rückert C, Weger-Lucarelli J, Garcia-Luna S et al. 2017. Mosquitoes transmit unique West Nile virus populations during each feeding episode. Cell Rep 19:4709–18
    [Google Scholar]
  72. 72. 
    Wang W-K, Lin S-R, Lee C-M, King C-C, Chang S-C 2002. Dengue type 3 virus in plasma is a population of closely related genomes: quasispecies. J. Virol. 76:94662–65
    [Google Scholar]
  73. 73. 
    Holmes EC. 2003. Patterns of intra- and interhost nonsynonymous variation reveal strong purifying selection in dengue virus. J. Virol. 77:2011296–98
    [Google Scholar]
  74. 74. 
    Tu Z, He Y, Lu H, Xu L, Yang Z et al. 2013. Mutant spectrum of dengue type 1 virus in the plasma of patients from the 2006 epidemic in South China. Int. J. Infect. Dis. 17:11e1080–1080
    [Google Scholar]
  75. 75. 
    Lin S-R, Hsieh S-C, Yueh Y-Y, Lin T-H, Chao D-Y et al. 2004. Study of sequence variation of dengue type 3 virus in naturally infected mosquitoes and human hosts: implications for transmission and evolution. J. Virol. 78:2212717–21
    [Google Scholar]
  76. 76. 
    Descloux E, Cao-Lormeau V-M, Roche C, De Lamballerie X 2009. Dengue 1 diversity and microevolution, French Polynesia 2001–2006: connection with epidemiology and clinics. PLOS Negl. Trop. Dis. 3:8e493
    [Google Scholar]
  77. 77. 
    Sessions OM, Wilm A, Kamaraj US, Choy MM, Chow A et al. 2015. Analysis of dengue virus genetic diversity during human and mosquito infection reveals genetic constraints. PLOS Negl. Trop. Dis. 9:9e0004044
    [Google Scholar]
  78. 78. 
    Gorzer I, Guelly C, Trajanoski S, Puchhammer-Stockl E 2010. Deep sequencing reveals highly complex dynamics of human cytomegalovirus genotypes in transplant patients over time. J. Virol. 84:147195–203
    [Google Scholar]
  79. 79. 
    Renzette N, Bhattacharjee B, Jensen JD, Gibson L, Kowalik TF 2011. Extensive genome-wide variability of human cytomegalovirus in congenitally infected infants. PLOS Pathog 7:5e1001344
    [Google Scholar]
  80. 80. 
    Cudini J, Roy S, Houldcroft CJ, Bryant JM, Depledge DP et al. 2019. Human cytomegalovirus haplotype reconstruction reveals high diversity due to superinfection and evidence of within-host recombination. PNAS 116:125693–98
    [Google Scholar]
  81. 81. 
    Pokalyuk C, Renzette N, Irwin KK, Pfeifer SP, Gibson L et al. 2017. Characterizing human cytomegalovirus reinfection in congenitally infected infants: an evolutionary perspective. Mol. Ecol. 26:71980–90
    [Google Scholar]
  82. 82. 
    Lassalle F, Depledge DP, Reeves MB, Brown AC, Christiansen MT et al. 2016. Islands of linkage in an ocean of pervasive recombination reveals two-speed evolution of human cytomegalovirus genomes. Virus Evol 2:1vew017
    [Google Scholar]
  83. 83. 
    Domingo E, Martín V, Perales C, Grande-Pérez A, García-Arriaza J, Arias A 2006. Viruses as quasispecies: biological implications. Quasispecies: Concept and Implications for Virology E Domingo 51–82 Berlin/Heidelberg: Springer
    [Google Scholar]
  84. 84. 
    Holland J, Spindler K, Horodyski F, Grabau E, Nichol S, VandePol S 1982. Rapid evolution of RNA genomes. Science 215:45401577–85
    [Google Scholar]
  85. 85. 
    Bull JJ, Meyers LA, Lachmann M 2005. Quasispecies made simple. PLOS Comput. Biol 1:6e61
    [Google Scholar]
  86. 86. 
    Domingo E, Sheldon J, Perales C 2012. Viral quasispecies evolution. Microbiol. Mol. Biol. Rev. 76:2159–216
    [Google Scholar]
  87. 87. 
    Poirier EZ, Vignuzzi M. 2017. Virus population dynamics during infection. Curr. Opin. Virol. 23:82–87
    [Google Scholar]
  88. 88. 
    Domingo E, Holland JJ. 1997. RNA virus mutations and fitness for survival. Annu. Rev. Microbiol. 51:151–78
    [Google Scholar]
  89. 89. 
    Whitfield ZJ, Andino R. 2016. Characterization of viral populations by using circular sequencing. J. Virol. 90:208950–53
    [Google Scholar]
  90. 90. 
    Biebricher CK, Eigen M. 2006. What is a quasispecies. ? Curr. Top. Microbiol. Immunol. 299:1–31
    [Google Scholar]
  91. 91. 
    Roossinck MJ, Schneider WL. 2006. Mutant clouds and occupation of sequence space in plant RNA viruses. Quasispecies: Concept and Implications for Virology E Domingo 337–48 Berlin/Heidelberg: Springer
    [Google Scholar]
  92. 92. 
    Moya A, Elena SF, Bracho A, Miralles R, Barrio E 2000. The evolution of RNA viruses: a population genetics view. PNAS 97:136967–73
    [Google Scholar]
  93. 93. 
    Jenkins GM, Worobey M, Woelk CH, Holmes EC 2001. Evidence for the non-quasispecies evolution of RNA viruses. Mol. Biol. Evol. 18:6987–94
    [Google Scholar]
  94. 94. 
    Wilke CO. 2005. Quasispecies theory in the context of population genetics. BMC Evol. Biol. 5:144
    [Google Scholar]
  95. 95. 
    Pfeiffer JK, Kirkegaard K. 2003. A single mutation in poliovirus RNA-dependent RNA polymerase confers resistance to mutagenic nucleotide analogs via increased fidelity. PNAS 100:127289–94
    [Google Scholar]
  96. 96. 
    Pfeiffer JK, Kirkegaard K. 2005. Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice. PLOS Pathog 1:2e11
    [Google Scholar]
  97. 97. 
    Gnadig NF, Beaucourt S, Campagnola G, Borderia AV, Sanz-Ramos M et al. 2012. Coxsackievirus B3 mutator strains are attenuated in vivo. PNAS 109:34E2294–2294
    [Google Scholar]
  98. 98. 
    Zeng J, Wang H, Xie X, Yang D, Zhou G, Yu L 2013. An increased replication fidelity mutant of foot-and-mouth disease virus retains fitness in vitro and virulence in vivo. Antivir. Res. 100:11–7
    [Google Scholar]
  99. 99. 
    Zeng J, Wang H, Xie X, Li C, Zhou G et al. 2014. Ribavirin-resistant variants of foot-and-mouth disease virus: the effect of restricted quasispecies diversity on viral virulence. J. Virol. 88:84008–20
    [Google Scholar]
  100. 100. 
    Sadeghipour S, McMinn PC. 2013. A study of the virulence in mice of high copying fidelity variants of human enterovirus 71. Virus Res 176:1/2265–72
    [Google Scholar]
  101. 101. 
    Rozen-Gagnon K, Stapleford KA, Mongelli V, Blanc H, Failloux A-B et al. 2014. Alphavirus mutator variants present host-specific defects and attenuation in mammalian and insect models. PLOS Pathog 10:1e1003877
    [Google Scholar]
  102. 102. 
    Cheung PPH, Watson SJ, Choy K-T, Fun Sia S, Wong DDY et al. 2014. Generation and characterization of influenza A viruses with altered polymerase fidelity. Nat. Commun. 5:14794
    [Google Scholar]
  103. 103. 
    Coffey LL, Beeharry Y, Borderia AV, Blanc H, Vignuzzi M 2011. Arbovirus high fidelity variant loses fitness in mosquitoes and mice. PNAS 108:3816038–43
    [Google Scholar]
  104. 104. 
    Regoes RR, Hamblin S, Tanaka MM 2013. Viral mutation rates: modelling the roles of within-host viral dynamics and the trade-off between replication fidelity and speed. Proc. R. Soc. B 280:175020122047
    [Google Scholar]
  105. 105. 
    Furio V, Moya A, Sanjuan R 2005. The cost of replication fidelity in an RNA virus. PNAS 102:2910233–37
    [Google Scholar]
  106. 106. 
    Fitzsimmons WJ, Woods RJ, McCrone JT, Woodman A, Arnold JJ et al. 2018. A speed–fidelity trade-off determines the mutation rate and virulence of an RNA virus. PLOS Biol 16:6e2006459
    [Google Scholar]
  107. 107. 
    Furió V, Moya A, Sanjuán R 2007. The cost of replication fidelity in human immunodeficiency virus type 1. Proc. R. Soc. B 274:1607225–30
    [Google Scholar]
  108. 108. 
    Xiao Y, Dolan PT, Goldstein EF, Li M, Farkov M et al. 2017. Poliovirus intrahost evolution is required to overcome tissue-specific innate immune responses. Nat. Commun. 8:1375
    [Google Scholar]
  109. 109. 
    Pfeiffer JK, Kirkegaard K. 2006. Bottleneck-mediated quasispecies restriction during spread of an RNA virus from inoculation site to brain. PNAS 103:145520–25
    [Google Scholar]
  110. 110. 
    Kuss SK, Etheredge CA, Pfeiffer JK 2008. Multiple host barriers restrict poliovirus trafficking in mice. PLOS Pathog 4:6e1000082
    [Google Scholar]
  111. 111. 
    McCune BT, Lanahan MR, tenOever BR, Pfeiffer JK 2019. Rapid dissemination and monopolization of viral populations in mice revealed using a panel of barcoded viruses. J. Virol. 94:2e01590
    [Google Scholar]
  112. 112. 
    Aliota MT, Dudley DM, Newman CM, Weger-Lucarelli J, Stewart LM et al. 2018. Molecularly barcoded Zika virus libraries to probe in vivo evolutionary dynamics. PLOS Pathog 14:3e1006964
    [Google Scholar]
  113. 113. 
    Jabara CB, Jones CD, Roach J, Anderson JA, Swanstrom R 2011. Accurate sampling and deep sequencing of the HIV-1 protease gene using a primer ID. PNAS 108:5020166–71
    [Google Scholar]
  114. 114. 
    Schmitt MW, Kennedy SR, Salk JJ, Fox EJ, Hiatt JB, Loeb LA 2012. Detection of ultra-rare mutations by next-generation sequencing. PNAS 109:3614508–13
    [Google Scholar]
/content/journals/10.1146/annurev-virology-010320-061642
Loading
/content/journals/10.1146/annurev-virology-010320-061642
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error