1932

Abstract

RNA viruses are unique in their evolutionary capacity, exhibiting high mutation rates and frequent recombination. They rapidly adapt to environmental changes, such as shifts in immune pressure or pharmacological challenge. The evolution of RNA viruses has been brought into new focus with the recent developments of genetic and experimental tools to explore and manipulate the evolutionary dynamics of viral populations. These studies have uncovered new mechanisms that enable viruses to overcome evolutionary challenges in the environment and have emphasized the intimate relationship of viral populations with evolution. Here, we review some of the emerging viral and host mechanisms that underlie the evolution of RNA viruses. We also discuss new studies that demonstrate that the relationship between evolutionary dynamics and virus biology spans many spatial and temporal scales, affecting transmission dynamics within and between hosts as well as pathogenesis.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-101416-041718
2018-09-29
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/virology/5/1/annurev-virology-101416-041718.html?itemId=/content/journals/10.1146/annurev-virology-101416-041718&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Duffy S, Shackelton LA, Holmes EC 2008. Rates of evolutionary change in viruses: patterns and determinants. Nat. Rev. Genet. 9:267–76
    [Google Scholar]
  2. 2.  Sanjuan R, Nebot MR, Chirico N, Mansky LM, Belshaw R 2010. Viral mutation rates. J. Virol. 84:9733–48
    [Google Scholar]
  3. 3.  Suttle CA 2007. Marine viruses—major players in the global ecosystem. Nat. Rev. Microbiol. 5:801–12
    [Google Scholar]
  4. 4.  Elde NC, Child SJ, Geballe AP, Malik HS 2009. Protein kinase R reveals an evolutionary model for defeating viral mimicry. Nature 457:485–89
    [Google Scholar]
  5. 5.  Enard D, Cai L, Gwennap C, Petrov DA 2016. Viruses are a dominant driver of protein adaptation in mammals. eLife 5:e12469
    [Google Scholar]
  6. 6.  Demogines A, Abraham J, Choe H, Farzan M, Sawyer SL 2013. Dual host-virus arms races shape an essential housekeeping protein. PLOS Biol 11:e1001571
    [Google Scholar]
  7. 7.  Drake JW 1993. Rates of spontaneous mutation among RNA viruses. PNAS 90:4171–75
    [Google Scholar]
  8. 8.  Sanjuán R 2012. From molecular genetics to phylodynamics: evolutionary relevance of mutation rates across viruses. PLOS Pathog 8:e1002685
    [Google Scholar]
  9. 9.  Lynch M 2010. Evolution of the mutation rate. Trends Genet 26:345–52
    [Google Scholar]
  10. 10.  Sanjuán R, Domingo-Calap P 2016. Mechanisms of viral mutation. Cell. Mol. Life Sci. 73:4433–48
    [Google Scholar]
  11. 11.  Luria SE, Delbrück M 1943. Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28:491–511
    [Google Scholar]
  12. 12.  Korboukh VK, Lee CA, Acevedo A, Vignuzzi M, Xiao Y et al. 2014. RNA virus population diversity, an optimum for maximal fitness and virulence. J. Biol. Chem. 289:29531–44
    [Google Scholar]
  13. 13.  Acevedo A, Brodsky L, Andino R 2014. Mutational and fitness landscapes of an RNA virus revealed through population sequencing. Nature 505:686–90
    [Google Scholar]
  14. 14.  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]
  15. 15.  Zhou S, Jones C, Mieczkowski P, Swanstrom R 2015. Primer ID validates template sampling depth and greatly reduces the error rate of next-generation sequencing of HIV-1 genomic RNA populations. J. Virol. 89:8540–55
    [Google Scholar]
  16. 16.  Acevedo A, Andino R 2014. Library preparation for highly accurate population sequencing of RNA viruses. Nat. Protoc. 9:1760–69
    [Google Scholar]
  17. 17.  Whitfield ZJ, Andino R 2016. Characterization of viral populations by using circular sequencing. J. Virol. 90:8950–53
    [Google Scholar]
  18. 18.  Harris RS, Dudley JP 2015. APOBECs and virus restriction. Virology 479–80:131–45
    [Google Scholar]
  19. 19.  Tomaselli S, Galeano F, Locatelli F, Gallo A 2015. ADARs and the balance game between virus infection and innate immune cell response. Curr. Issues Mol. Biol. 17:37–51
    [Google Scholar]
  20. 20.  Tenoever BR, Ng SL, Chua MA, McWhirter SM, García-Sastre A, Maniatis T 2007. Multiple functions of the IKK-related kinase IKKε in interferon-mediated antiviral immunity. Science 315:1274–78
    [Google Scholar]
  21. 21.  Suspène R, Renard M, Henry M, Guétard D, Puyraimond-Zemmour D et al. 2008. Inversing the natural hydrogen bonding rule to selectively amplify GC-rich ADAR-edited RNAs. Nucleic Acids Res 36:e72
    [Google Scholar]
  22. 22.  Ward SV, George CX, Welch MJ, Liou LY, Hahm B et al. 2011. RNA editing enzyme adenosine deaminase is a restriction factor for controlling measles virus replication that also is required for embryogenesis. PNAS 108:331–36
    [Google Scholar]
  23. 23.  Cattaneo R, Schmid A, Eschle D, Baczko K, ter Meulen V, Billeter MA 1988. Biased hypermutation and other genetic changes in defective measles viruses in human brain infections. Cell 55:255–65
    [Google Scholar]
  24. 24.  Carpenter JA, Keegan LP, Wilfert L, O'Connell MA, Jiggins FM 2009. Evidence for ADAR-induced hypermutation of the Drosophila sigma virus (Rhabdoviridae). BMC Genet 10:1–7
    [Google Scholar]
  25. 25.  Piontkivska H, Frederick M, Miyamoto MM, Wayne ML 2017. RNA editing by the host ADAR system affects the molecular evolution of the Zika virus. Ecol. Evol. 7:4475–85
    [Google Scholar]
  26. 26.  Khrustalev VV, Khrustaleva TA, Sharma N, Giri R 2017. Mutational pressure in Zika virus: local ADAR-editing areas associated with pauses in translation and replication. Front. Cell. Infect. Microbiol. 7:44
    [Google Scholar]
  27. 27.  Khrustalev VV, Barkovsky EV, Khrustaleva TA 2015. Local mutational pressures in genomes of Zaire ebolavirus and Marburg virus. Adv. Bioinform. 2015:678587
    [Google Scholar]
  28. 28.  Shabman RS, Jabado OJ, Mire CE, Stockwell TB, Edwards M et al. 2014. Deep sequencing identifies noncanonical editing of Ebola and Marburg virus RNAs in infected cells. mBio 5:e02011
    [Google Scholar]
  29. 29.  Dudas G, Carvalho LM, Bedford T, Tatem AJ, Baele G et al. 2017. Virus genomes reveal factors that spread and sustained the Ebola epidemic. Nature 544:309–15
    [Google Scholar]
  30. 30.  Park DJ, Dudas G, Wohl S, Goba A, Whitmer SLM et al. 2015. Ebola virus epidemiology, transmission, and evolution during seven months in Sierra Leone. Cell 161:1516–26
    [Google Scholar]
  31. 31.  Tong YG, Shi WF, Liu D, Qian J, Liang L et al. 2015. Genetic diversity and evolutionary dynamics of Ebola virus in Sierra Leone. Nature 524:93–96
    [Google Scholar]
  32. 32.  Whitmer SLM, Ladner JT, Wiley MR, Patel K, Dudas G et al. 2018. Active Ebola virus replication and heterogeneous evolutionary rates in EVD survivors. Cell Rep 22:1159–68
    [Google Scholar]
  33. 33.  Ni M, Chen C, Qian J, Xiao HX, Shi WF et al. 2016. Intra-host dynamics of Ebola virus during 2014. Nat. Microbiol. 1:16151
    [Google Scholar]
  34. 34.  Samuel CE 2011. Adenosine deaminases acting on RNA (ADARs) are both antiviral and proviral. Virology 411:180–93
    [Google Scholar]
  35. 35.  Toth AM, Li Z, Cattaneo R, Samuel CE 2009. RNA-specific adenosine deaminase ADAR1 suppresses measles virus-induced apoptosis and activation of protein kinase PKR. J. Biol. Chem. 284:29350–56
    [Google Scholar]
  36. 36.  de Chassey B, Aublin-Gex A, Ruggieri A, Meyniel-Schicklin L, Pradezynski F et al. 2013. The interactomes of influenza virus NS1 and NS2 proteins identify new host factors and provide insights for ADAR1 playing a supportive role in virus replication. PLOS Pathog 9:e1003440
    [Google Scholar]
  37. 37.  Sanjuán R, Moya A, Elena SF 2004. The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. PNAS 101:8396–401
    [Google Scholar]
  38. 38.  Vale PF, Choisy M, Froissart R, Sanjuán R, Gandon S 2012. The distribution of mutational fitness effects of phage φX174 on different hosts. Evolution 66:3495–507
    [Google Scholar]
  39. 39.  Visher E, Whitefield SE, McCrone JT, Fitzsimmons W, Lauring AS 2016. The mutational robustness of influenza A virus. PLOS Pathog 12:e1005856
    [Google Scholar]
  40. 40.  Wright S 1955. Classification of the factors of evolution. Cold Spring Harb. Symp. Quant. Biol. 20:16–24
    [Google Scholar]
  41. 41.  Gillespie JH 2001. Is the population size of a species relevant to its evolution?. Evolution 55:2161–69
    [Google Scholar]
  42. 42.  Muller HJ 1932. Some genetic aspects of sex. Am. Nat. 66:118–38
    [Google Scholar]
  43. 43.  Muller HJ 1964. The relation of recombination to mutational advance. Mutat. Res. 106:2–9
    [Google Scholar]
  44. 44.  Felsenstein J 1974. The evolutionary advantage of recombination. Genetics 78:737–56
    [Google Scholar]
  45. 45.  Gerrish PJ, Lenski RE 1998. The fate of competing beneficial mutations in an asexual population. Genetica 102–3:127–44
    [Google Scholar]
  46. 46.  Kirkegaard K, Baltimore D 1986. The mechanism of RNA recombination in poliovirus. Cell 47:433–43
    [Google Scholar]
  47. 47.  Kempf BJ, Peersen OB, Barton DJ 2016. Poliovirus polymerase Leu420 facilitates RNA recombination and ribavirin resistance. J. Virol. 90:8410–21
    [Google Scholar]
  48. 48.  Xiao Y, Rouzine IM, Bianco S, Acevedo A, Goldstein EF et al. 2016. RNA recombination enhances adaptability and is required for virus spread and virulence. Cell Host Microbe 19:493–503
    [Google Scholar]
  49. 49.  Chao L 1990. Fitness of RNA virus decreased by Muller's ratchet. Nature 348:454–55
    [Google Scholar]
  50. 50.  Chao L, Tran T, Matthews C 1992. Muller's ratchet and the advantage of sex in the RNA virus φ6. Evolution 46:289–99
    [Google Scholar]
  51. 51.  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. 8:375
    [Google Scholar]
  52. 52.  Oberste MS, Maher K, Kilpatrick DR, Pallansch MA 1999. Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J. Virol. 73:1941–48
    [Google Scholar]
  53. 53.  Pons-Salort M, Parker EPK, Grassly NC 2015. The epidemiology of non-polio enteroviruses: recent advances and outstanding questions. Curr. Opin. Infect. Dis. 28:479–87
    [Google Scholar]
  54. 54.  Yip CCY, Lau SKP, Woo PCY, Yuen KY 2013. Human enterovirus 71 epidemics: What's next?. Emerg. Health Threats J. 6:19780
    [Google Scholar]
  55. 55.  Oberste MS, Maher K, Pallansch MA 2004. Evidence for frequent recombination within species human enterovirus B based on complete genomic sequences of all thirty-seven serotypes. J. Virol. 78:855–67
    [Google Scholar]
  56. 56.  Oberste MS, Peñaranda S, Pallansch MA 2004. RNA recombination plays a major role in genomic change during circulation of coxsackie B viruses. J. Virol. 78:2948–55
    [Google Scholar]
  57. 57.  Stern A, Yeh MT, Zinger T, Smith M, Wright C et al. 2017. The evolutionary pathway to virulence of an RNA virus. Cell 169:35–46
    [Google Scholar]
  58. 58.  Guillot S, Caro V, Cuervo N, Korotkova E, Combiescu M et al. 2000. Natural genetic exchanges between vaccine and wild poliovirus strains in humans. J. Virol. 74:8434–43
    [Google Scholar]
  59. 59.  Lazzarini RA, Keene JD, Schubert M 1981. The origins of defective interfering particles of the negative-strand RNA viruses. Cell 26:Pt. 2145–54
    [Google Scholar]
  60. 60.  Li D, Lott WB, Lowry K, Jones A, Thu HM, Aaskov J 2011. Defective interfering viral particles in acute dengue infections. PLOS ONE 6:e19447
    [Google Scholar]
  61. 61.  Li D, Aaskov J 2014. Sub-genomic RNA of defective interfering (D.I.) dengue viral particles is replicated in the same manner as full length genomes. Virology 468–70:248–55
    [Google Scholar]
  62. 62.  Šantak M, Markušić M, Balija ML, Kopač SK, Jug R et al. 2015. Accumulation of defective interfering viral particles in only a few passages in Vero cells attenuates mumps virus neurovirulence. Microbes Infect 17:228–36
    [Google Scholar]
  63. 63.  Amesse LS, Pridgen CL, Kingsbury DW 1982. Sendai virus DI RNA species with conserved virus genome termini and extensive internal deletions. Virology 118:17–27
    [Google Scholar]
  64. 64.  Pattnaik AK, Ball LA, LeGrone AW, Wertz GW 1992. Infectious defective interfering particles of VSV from transcripts of a cDNA clone. Cell 69:1011–20
    [Google Scholar]
  65. 65.  Bujarski JJ, Kaesberg P 1986. Genetic recombination between RNA components of a multipartite plant virus. Nature 321:528–31
    [Google Scholar]
  66. 66.  Shivakoti R, Siwek M, Hauer D, Schultz KLW, Griffin DE 2013. Induction of dendritic cell production of type I and type III interferons by wild-type and vaccine strains of measles virus: role of defective interfering RNAs. J. Virol. 87:7816–27
    [Google Scholar]
  67. 67.  Frensing T 2015. Defective interfering viruses and their impact on vaccines and viral vectors. Biotechnol. J. 10:681–89
    [Google Scholar]
  68. 68.  Poirier EZ, Mounce BC, Rozen-Gagnon K, Hooikaas PJ, Stapleford KA et al. 2016. Low-fidelity polymerases of alphaviruses recombine at higher rates to overproduce defective interfering particles. J. Virol. 90:2446–54
    [Google Scholar]
  69. 69.  McDonald SM, Nelson MI, Turner PE, Patton JT 2016. Reassortment in segmented RNA viruses: mechanisms and outcomes. Nat. Rev. Microbiol. 14:448–60
    [Google Scholar]
  70. 70.  Vijaykrishna D, Mukerji R, Smith GJD 2015. RNA virus reassortment: an evolutionary mechanism for host jumps and immune evasion. PLOS Pathog 11:e1004902
    [Google Scholar]
  71. 71.  Worobey M, Han GZ, Rambaut A 2014. A synchronized global sweep of the internal genes of modern avian influenza virus. Nature 508:254–57
    [Google Scholar]
  72. 72.  Westgeest KB, Russell CA, Lin X, Spronken MIJ, Bestebroer TM et al. 2014. Genomewide analysis of reassortment and evolution of human influenza A(H3N2) viruses circulating between 1968 and 2011. J. Virol. 88:2844–57
    [Google Scholar]
  73. 73.  Scholtissek C 2002. Pandemic influenza: antigenic shift. Perspect. Med. Virol 7:87–100
    [Google Scholar]
  74. 74.  Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S et al. 2009. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325:197–201
    [Google Scholar]
  75. 75.  Haldane JBS 1927. A mathematical theory of natural and artificial selection. Part V. Selection and mutation. Math. Proc. Cambridge Philos. Soc. 23:838–44
    [Google Scholar]
  76. 76.  Goyal S, Balick DJ, Jerison ER, Neher RA, Shraiman BI, Desai MM 2012. Dynamic mutation-selection balance as an evolutionary attractor. Genetics 191:1309–19
    [Google Scholar]
  77. 77.  Vignuzzi M, Stone JK, Andino R 2005. Ribavirin and lethal mutagenesis of poliovirus: molecular mechanisms, resistance and biological implications. Virus Res 107:173–81
    [Google Scholar]
  78. 78.  Crotty S, Cameron CE, Andino R 2001. RNA virus error catastrophe: direct molecular test by using ribavirin. PNAS 98:6895–900
    [Google Scholar]
  79. 79.  Pfeiffer JK, Kirkegaard K 2003. A single mutation in poliovirus RNA-dependent RNA polymerase confers resistance to mutagenic nucleotide analogs via increased fidelity. PNAS 100:7289–94
    [Google Scholar]
  80. 80.  Bull JJ, Sanjuán R, Wilke CO 2007. Theory of lethal mutagenesis for viruses. J. Virol. 81:2930–39
    [Google Scholar]
  81. 81.  Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R 2006. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439:344–48
    [Google Scholar]
  82. 82.  Stapleford KA, Rozen-Gagnon K, Das PK, Saul S, Poirier EZ et al. 2015. Viral polymerase-helicase complexes regulate replication fidelity to overcome intracellular nucleotide depletion. J. Virol. 89:11233–44
    [Google Scholar]
  83. 83.  McDonald S, Block A, Beaucourt S, Moratorio G, Vignuzzi M, Peersen OB 2016. Design of a genetically stable high fidelity coxsackievirus B3 polymerase that attenuates virus growth in vivo. J. Biol. Chem. 291:13999–4011
    [Google Scholar]
  84. 84.  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. 88:4008–20
    [Google Scholar]
  85. 85.  Gnädig NF, Beaucourt S, Campagnola G, Bordería AV, Sanz-Ramos M et al. 2012. Coxsackievirus B3 mutator strains are attenuated in vivo. PNAS 109:E2294–303
    [Google Scholar]
  86. 86.  Rozen-Gagnon K, Stapleford KA, Mongelli V, Blanc H, Failloux AB et al. 2014. Alphavirus mutator variants present host-specific defects and attenuation in mammalian and insect models. PLOS Pathog 10:e1003877
    [Google Scholar]
  87. 87.  Gao Q, Palese P 2009. Rewiring the RNAs of influenza virus to prevent reassortment. PNAS 106:15891–96
    [Google Scholar]
  88. 88.  Arnold JJ, Vignuzzi M, Stone JK, Andino R, Cameron CE 2005. Remote site control of an active site fidelity checkpoint in a viral RNA-dependent RNA polymerase. J. Biol. Chem. 280:25706–16
    [Google Scholar]
  89. 89.  Campagnola G, McDonald S, Beaucourt S, Vignuzzi M, Peersen OB 2015. Structure-function relationships underlying the replication fidelity of viral RNA-dependent RNA polymerases. J. Virol. 89:275–86
    [Google Scholar]
  90. 90.  Pfeiffer JK, Kirkegaard K 2005. Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice. PLOS Pathog 1:e11
    [Google Scholar]
  91. 91.  Vignuzzi M, Wendt E, Andino R 2008. Engineering attenuated virus vaccines by controlling replication fidelity. Nat. Med. 14:154–61
    [Google Scholar]
  92. 92.  Lauring AS, Jones JO, Andino R 2010. Rationalizing the development of live attenuated virus vaccines. Nat. Biotechnol. 28:573–79
    [Google Scholar]
  93. 93.  Weeks SA, Lee CA, Zhao Y, Smidansky ED, August A et al. 2012. A polymerase mechanism-based strategy for viral attenuation and vaccine development. J. Biol. Chem. 287:31618–22
    [Google Scholar]
  94. 94.  Pena L, Sutton T, Chockalingam A, Kumar S, Angel M et al. 2013. Influenza viruses with rearranged genomes as live-attenuated vaccines. J. Virol. 87:5118–27
    [Google Scholar]
  95. 95.  Smith EC, Blanc H, Surdel MC, Vignuzzi M, Denison MR 2013. Coronaviruses lacking exoribonuclease activity are susceptible to lethal mutagenesis: evidence for proofreading and potential therapeutics. PLOS Pathog 9:e1003565
    [Google Scholar]
  96. 96.  Wilke CO, Wang JL, Ofria C, Lenski RE, Adami C 2001. Evolution of digital organisms at high mutation rates leads to survival of the flattest. Nature 412:331–33
    [Google Scholar]
  97. 97.  Krakauer DC, Plotkin JB 2002. Redundancy, antiredundancy, and the robustness of genomes. PNAS 99:1405–9
    [Google Scholar]
  98. 98.  Dennehy JJ, Duffy S, O'Keefe KJ, Edwards SV, Turner PE 2013. Frequent coinfection reduces RNA virus population genetic diversity. J. Hered. 104:704–12
    [Google Scholar]
  99. 99.  Goldhill D, Lee A, Williams ES, Turner PE 2014. Evolvability and robustness in populations of RNA virus φ6. Front. Microbiol. 5:35
    [Google Scholar]
  100. 100.  Novella IS, Presloid JB, Zhou T, Smith-Tsurkan SD, Ebendick-Corpus BE et al. 2010. Genomic evolution of vesicular stomatitis virus strains with differences in adaptability. J. Virol. 84:4960–68
    [Google Scholar]
  101. 101.  de Visser JAGM, Hermisson J, Wagner GP, Ancel Meyers L, Bagheri-Chaichian H et al. 2003. Perspective: evolution and detection of genetic robustness. Evolution 57:1959–72
    [Google Scholar]
  102. 102.  Elena SF, Carrasco P, Daròs JA, Sanjuán R 2006. Mechanisms of genetic robustness in RNA viruses. EMBO Rep 7:168–73
    [Google Scholar]
  103. 103.  Lauring AS, Frydman J, Andino R 2013. The role of mutational robustness in RNA virus evolution. Nat. Rev. Microbiol. 11:327–36
    [Google Scholar]
  104. 104.  Cuevas JM, Moya A, Sanjuán R 2009. A genetic background with low mutational robustness is associated with increased adaptability to a novel host in an RNA virus. J. Evol. Biol. 22:2041–48
    [Google Scholar]
  105. 105.  Tokuriki N, Tawfik DS 2009. Stability effects of mutations and protein evolvability. Curr. Opin. Struct. Biol. 19:596–604
    [Google Scholar]
  106. 106.  Tokuriki N, Oldfield CJ, Uversky VN, Berezovsky IN, Tawfik DS 2009. Do viral proteins possess unique biophysical features?. Trends Biochem. Sci. 34:53–59
    [Google Scholar]
  107. 107.  Tokuriki N, Tawfik DS 2009. Protein dynamism and evolvability. Science 324:203–7
    [Google Scholar]
  108. 108.  Villordo SM, Filomatori CV, Sánchez-Vargas I, Blair CD, Gamarnik AV 2015. Dengue virus RNA structure specialization facilitates host adaptation. PLOS Pathog 11:e1004604
    [Google Scholar]
  109. 109.  Mueller S, Papamichail D, Coleman JR, Skiena S, Wimmer E 2006. Reduction of the rate of poliovirus protein synthesis through large-scale codon deoptimization causes attenuation of viral virulence by lowering specific infectivity. J. Virol. 80:9687–96
    [Google Scholar]
  110. 110.  Lauring AS, Acevedo A, Cooper SB, Andino R 2012. Codon usage determines the mutational robustness, evolutionary capacity, and virulence of an RNA virus. Cell Host Microbe 12:623–32
    [Google Scholar]
  111. 111.  Moratorio G, Henningsson R, Barbezange C, Carrau L, Bordería AV et al. 2017. Attenuation of RNA viruses by redirecting their evolution in sequence space. Nat. Microbiol. 2:17088
    [Google Scholar]
  112. 112.  Geller R, Taguwa S, Frydman J 2012. Broad action of Hsp90 as a host chaperone required for viral replication. Biochim. Biophys. Acta 1823:698–706
    [Google Scholar]
  113. 113.  Taguwa S, Maringer K, Li X, Bernal-Rubio D, Rauch JN et al. 2015. Defining Hsp70 subnetworks in dengue virus replication reveals key vulnerability in flavivirus infection. Cell 163:1108–23
    [Google Scholar]
  114. 114.  Macejak DG, Sarnow P 1992. Association of heat shock protein 70 with enterovirus capsid precursor P1 in infected human cells. J. Virol. 66:1520–27
    [Google Scholar]
  115. 115.  Sagara J, Kawai A 1992. Identification of heat shock protein 70 in the rabies virion. Virology 190:845–48
    [Google Scholar]
  116. 116.  Geller R, Pechmann S, Acevedo A, Andino R, Frydman J 2018. Hsp90 shapes protein and RNA evolution to balance trade-offs between protein stability and aggregation. Nat. Commun. 9:11781
    [Google Scholar]
  117. 117.  Geller R, Vignuzzi M, Andino R, Frydman J 2007. Evolutionary constraints on chaperone-mediated folding provide an antiviral approach refractory to development of drug resistance. Genes Dev 21:195–205
    [Google Scholar]
  118. 118.  Geller R, Andino R, Frydman J 2013. Hsp90 inhibitors exhibit resistance-free antiviral activity against respiratory syncytial virus. PLOS ONE 8:e56762
    [Google Scholar]
  119. 119.  Gilmore R, Coffey MC, Lee PWK 1998. Active participation of Hsp90 in the biogenesis of the trimeric reovirus cell attachment protein ς1. J. Biol. Chem. 273:15227–33
    [Google Scholar]
  120. 120.  Hong S, Choi G, Park S, Chung AS, Hunter E, Rhee SS 2001. Type D retrovirus Gag polyprotein interacts with the cytosolic chaperonin TRiC. J. Virol. 75:2526–34
    [Google Scholar]
  121. 121.  Inoue Y, Aizaki H, Hara H, Matsuda M, Ando T et al. 2011. Chaperonin TRiC/CCT participates in replication of hepatitis C virus genome via interaction with the viral NS5B protein. Virology 410:38–47
    [Google Scholar]
  122. 122.  Zhang J, Wu X, Zan J, Wu Y, Ye C et al. 2013. Cellular chaperonin CCTγ contributes to rabies virus replication during infection. J. Virol. 87:7608–21
    [Google Scholar]
  123. 123.  Phillips AM, Gonzalez LO, Nekongo EE, Ponomarenko AI, McHugh SM et al. 2017. Host proteostasis modulates influenza evolution. eLife 6:e28652
    [Google Scholar]
  124. 124.  Eigen M 1971. Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften 58:465–523
    [Google Scholar]
  125. 125.  Eigen M 1996. On the nature of virus quasispecies. Trends Microbiol 4:216–18
    [Google Scholar]
  126. 126.  Wilke CO 2005. Quasispecies theory in the context of population genetics. BMC Evol. Biol. 5:44
    [Google Scholar]
  127. 127.  Novella IS, Reissig DD, Wilke CO 2004. Density-dependent selection in vesicular stomatitis virus. J. Virol. 78:5799–804
    [Google Scholar]
  128. 128.  Shirogane Y, Watanabe S, Yanagi Y 2016. Cooperative interaction within RNA virus mutant spectra. Curr. Top. Microbiol. Immunol. 392:219–29
    [Google Scholar]
  129. 129.  Díaz-Muñoz SL, Sanjuán R, West S 2017. Sociovirology: conflict, cooperation, and communication among viruses. Cell Host Microbe 22:437–41
    [Google Scholar]
  130. 130.  Ciota AT, Ehrbar DJ, Van Slyke GA, Willsey GG, Kramer LD 2012. Cooperative interactions in the West Nile virus mutant swarm. BMC Evol. Biol. 12:58
    [Google Scholar]
  131. 131.  Shirogane Y, Watanabe S, Yanagi Y 2012. Cooperation between different RNA virus genomes produces a new phenotype. Nat. Commun. 3:1235
    [Google Scholar]
  132. 132.  Xue KS, Hooper KA, Ollodart AR, Dingens AS, Bloom JD 2016. Cooperation between distinct viral variants promotes growth of H3N2 influenza in cell culture. eLife 5:e13974
    [Google Scholar]
  133. 133.  Bordería AV, Isakov O, Moratorio G, Henningsson R, Agüera-González S et al. 2015. Group selection and contribution of minority variants during virus adaptation determines virus fitness and phenotype. PLOS Pathog 11:e1004838
    [Google Scholar]
  134. 134.  Cao L, Wu C, Shi H, Gong Z, Zhang E et al. 2014. Coexistence of hepatitis B virus quasispecies enhances viral replication and the ability to induce host antibody and cellular immune responses. J. Virol. 88:8656–66
    [Google Scholar]
  135. 135.  Ke R, Aaskov J, Holmes EC, Lloyd-Smith JO 2013. Phylodynamic analysis of the emergence and epidemiological impact of transmissible defective dengue viruses. PLOS Pathog 9:e1003193
    [Google Scholar]
  136. 136.  Lin YP, Xiong X, Wharton SA, Martin SR, Coombs PJ et al. 2012. Evolution of the receptor binding properties of the influenza A(H3N2) hemagglutinin. PNAS 109:21474–79
    [Google Scholar]
  137. 137.  Xue KS, Greninger AL, Pérez-Osorio A, Bloom JD 2018. Cooperating H3N2 influenza virus variants are not detectable in primary clinical samples. mSphere 3:e00552–17
    [Google Scholar]
  138. 138.  Nei M, Tajima F 1981. Genetic drift and estimation of effective population size. Genetics 98:625–40
    [Google Scholar]
  139. 139.  Pennings PS, Kryazhimskiy S, Wakeley J 2014. Loss and recovery of genetic diversity in adapting populations of HIV. PLOS Genet 10:e1004000
    [Google Scholar]
  140. 140.  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]
  141. 141.  Chen YH, Du W, Hagemeijer MC, Takvorian PM, Pau C et al. 2015. Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses. Cell 160:619–30
    [Google Scholar]
  142. 142.  Robinson CM, Jesudhasan PR, Pfeiffer JK 2014. Bacterial lipopolysaccharide binding enhances virion stability and promotes environmental fitness of an enteric virus. Cell Host Microbe 15:36–46
    [Google Scholar]
  143. 143.  Jones MK, Watanabe M, Zhu S, Graves CL, Keyes LR et al. 2014. Enteric bacteria promote human and mouse norovirus infection of B cells. Science 346:755–59
    [Google Scholar]
  144. 144.  Erickson AK, Jesudhasan PR, Mayer MJ, Narbad A, Winter SE, Pfeiffer JK 2018. Bacteria facilitate enteric virus co-infection of mammalian cells and promote genetic recombination. Cell Host Microbe 23:77–88
    [Google Scholar]
  145. 145.  Aguilera ER, Erickson AK, Jesudhasan PR, Robinson CM, Pfeiffer JK 2017. Plaques formed by mutagenized viral populations have elevated coinfection frequencies. mBio 8:e02020–16
    [Google Scholar]
  146. 146.  Ramakrishnaiah V, Thumann C, Fofana I, Habersetzer F, Pan Q et al. 2013. Exosome-mediated transmission of hepatitis C virus between human hepatoma Huh7.5 cells. PNAS 110:13109–13
    [Google Scholar]
  147. 147.  Longatti A, Boyd B, Chisari FV 2015. Virion-independent transfer of replication-competent hepatitis C virus RNA between permissive cells. J. Virol. 89:2956–61
    [Google Scholar]
  148. 148.  Lawrence DM, Patterson CE, Gales TL, D'Orazio JL, Vaughn MM, Rall GF 2000. Measles virus spread between neurons requires cell contact but not CD46 expression, syncytium formation, or extracellular virus production. J. Virol. 74:1908–18
    [Google Scholar]
  149. 149.  Chen P, Hübner W, Spinelli MA, Chen BK 2007. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J. Virol. 81:12582–95
    [Google Scholar]
  150. 150.  Sanjuán R 2017. Collective infectious units in viruses. Trends Microbiol 25:402–12
    [Google Scholar]
  151. 151.  Altan-Bonnet N 2017. Lipid tales of viral replication and transmission. Trends Cell Biol 27:201–13
    [Google Scholar]
  152. 152.  Nagashima S, Jirintai S, Takahashi M, Kobayashi T, Tanggis et al. 2014. Hepatitis E virus egress depends on the exosomal pathway, with secretory exosomes derived from multivesicular bodies. J. Gen. Virol. 95:Pt. 102166–75
    [Google Scholar]
  153. 153.  Robinson SM, Tsueng G, Sin J, Mangale V, Rahawi S et al. 2014. Coxsackievirus B exits the host cell in shed microvesicles displaying autophagosomal markers. PLOS Pathog 10:e1004045
    [Google Scholar]
  154. 154.  Bird SW, Maynard ND, Covert MW, Kirkegaard K 2014. Nonlytic viral spread enhanced by autophagy components. PNAS 111:13081–86
    [Google Scholar]
  155. 155.  Feng Z, Hensley L, McKnight KL, Hu F, Madden V et al. 2013. A pathogenic picornavirus acquires an envelope by hijacking cellular membranes. Nature 496:367–71
    [Google Scholar]
  156. 156.  Gray RR, Parker J, Lemey P, Salemi M, Katzourakis A, Pybus OG 2011. The mode and tempo of hepatitis C virus evolution within and among hosts. BMC Evol. Biol. 11:131
    [Google Scholar]
  157. 157.  Wright S 1970. Random drift and the shifting balance theory of evolution. Mathematical Topics in Population Genetics1–31 Berlin: Springer
    [Google Scholar]
  158. 158.  Rotem A, Serohijos A, Chang C, Wolfe J, Fischer A et al. 2016. Tuning the course of evolution on the biophysical fitness landscape of an RNA virus Work. Pap. Harvard University Cambridge, MA:
  159. 159.  Moreno-Gamez S, Hill AL, Rosenbloom DIS, Petrov DA, Nowak MA, Pennings PS 2015. Imperfect drug penetration leads to spatial monotherapy and rapid evolution of multidrug resistance. PNAS 112:E2874–83
    [Google Scholar]
  160. 160.  Feder AF, Kline C, Polacino P, Cottrell M, Kashuba ADM et al. 2017. A spatio-temporal assessment of simian/human immunodeficiency virus (SHIV) evolution reveals a highly dynamic process within the host. PLOS Pathog 13:e1006358
    [Google Scholar]
  161. 161.  Hadfield J, Megill C, Bell SM, Huddleston J, Potter B et al. 2018. Nextstrain: real-time tracking of pathogen evolution. Bioinformatics. In press. https://doi.org/10.1093/bioinformatics/bty407
    [Crossref]
  162. 162.  Bloom JD, Raval A, Wilke CO 2007. Thermodynamics of neutral protein evolution. Genetics 175:255–66
    [Google Scholar]
  163. 163.  Wylie CS, Shakhnovich EI 2011. A biophysical protein folding model accounts for most mutational fitness effects in viruses. PNAS 108:9916–21
    [Google Scholar]
  164. 164.  Klein EY, Blumenkrantz D, Serohijos A, Shakhnovich E, Choi JM et al. 2018. Stability of the influenza virus hemagglutinin protein correlates with evolutionary dynamics. mSphere 3:e00554–17
    [Google Scholar]
  165. 165.  Bielejec F, Lemey P, Baele G, Rambaut A, Suchard MA 2014. Inferring heterogeneous evolutionary processes through time: from sequence substitution to phylogeography. Syst. Biol. 63:493–504
    [Google Scholar]
  166. 166.  Drummond AJ, Bouckaert RR 2015. Bayesian Evolutionary Analysis with BEAST Cambridge, UK: Cambridge Univ. Press
  167. 167.  Neher RA, Bedford T 2015. Nextflu: real-time tracking of seasonal influenza virus evolution in humans. Bioinformatics 31:3546–48
    [Google Scholar]
  168. 168.  Dellicour S, Rose R, Faria NR, Vieira LFP, Bourhy H et al. 2017. Using viral gene sequences to compare and explain the heterogeneous spatial dynamics of virus epidemics. Mol. Biol. Evol. 34:2563–71
    [Google Scholar]
  169. 169.  Greninger AL, Naccache SN, Federman S, Yu G, Mbala P et al. 2015. Rapid metagenomic identification of viral pathogens in clinical samples by real-time nanopore sequencing analysis. Genome Med 7:99
    [Google Scholar]
  170. 170.  Hoenen T, Groseth A, Rosenke K, Fischer RJ, Hoenen A et al. 2016. Nanopore sequencing as a rapidly deployable Ebola outbreak tool. Emerg. Infect. Dis. 22:331–34
    [Google Scholar]
  171. 171.  Quick J, Grubaugh ND, Pullan ST, Claro IM, Smith AD et al. 2017. Multiplex PCR method for MinION and Illumina sequencing of Zika and other virus genomes directly from clinical samples. Nat. Protoc. 12:1261–76
    [Google Scholar]
  172. 172.  Hilton SK, Doud MB, Bloom JD 2017. phydms: software for phylogenetic analyses informed by deep mutational scanning. PeerJ 5:e3657
    [Google Scholar]
  173. 173.  Bloom JD 2017. Identification of positive selection in genes is greatly improved by using experimentally informed site-specific models. Biol. Direct. 12:1
    [Google Scholar]
  174. 174.  Stern A, Bianco S, Yeh MT, Wright C, Butcher K et al. 2014. Costs and benefits of mutational robustness in RNA viruses. Cell Rep 8:1026–36
    [Google Scholar]
  175. 175.  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]
  176. 176.  Ben-Shachar R, Koelle K 2015. Minimal within-host dengue models highlight the specific roles of the immune response in primary and secondary dengue infections. J. R. Soc. Interface 12:20140886
    [Google Scholar]
  177. 177.  Mordecai EA, Cohen JM, Evans MV, Gudapati P, Johnson LR et al. 2017. Detecting the impact of temperature on transmission of Zika, dengue, and chikungunya using mechanistic models. PLOS Negl. Trop. Dis. 11:e0005568
    [Google Scholar]
  178. 178.  Betancourt M, Fereres A, Fraile A, García-Arenal F 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]
  179. 179.  Moury B, Fabre F, Senoussi R 2007. Estimation of the number of virus particles transmitted by an insect vector. PNAS 104:17891–96
    [Google Scholar]
  180. 180.  Grubaugh ND, Smith DR, Brackney DE, Bosco-Lauth AM, Fauver JR et al. 2015. Experimental evolution of an RNA virus in wild birds: evidence for host-dependent impacts on population structure and competitive fitness. PLOS Pathog 11:e1004874
    [Google Scholar]
  181. 181.  Grubaugh ND, Rückert C, Armstrong PM, Bransfield A, Anderson JF et al. 2016. Transmission bottlenecks and RNAi collectively influence tick-borne flavivirus evolution. Virus Evol 2:vew033
    [Google Scholar]
  182. 182.  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 19:709–18
    [Google Scholar]
  183. 183.  McCrone JT, Lauring AS 2017. Genetic bottlenecks in intraspecies virus transmission. Curr. Opin. Virol. 28:20–25
    [Google Scholar]
  184. 184.  Novella IS, Clarke DK, Quer J, Duarte EA, Lee CH et al. 1995. Extreme fitness differences in mammalian and insect hosts after continuous replication of vesicular stomatitis virus in sandfly cells. J. Virol. 69:6805–9
    [Google Scholar]
  185. 185.  Smith-Tsurkan SD, Wilke CO, Novella IS 2010. Incongruent fitness landscapes, not tradeoffs, dominate the adaptation of vesicular stomatitis virus to novel host types. J. Gen. Virol. 91:Pt. 61484–93
    [Google Scholar]
  186. 186.  Lalić J, Cuevas JM, Elena SF 2011. Effect of host species on the distribution of mutational fitness effects for an RNA virus. PLOS Genet 7:e1002378
    [Google Scholar]
  187. 187.  Lalić J, Elena SF 2013. Epistasis between mutations is host-dependent for an RNA virus. Biol. Lett. 9:20120396
    [Google Scholar]
  188. 188.  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. 79:14253–60
    [Google Scholar]
  189. 189.  Stapleford KA, Coffey LL, Lay S, Bordería AV, Duong V et al. 2014. Emergence and transmission of arbovirus evolutionary intermediates with epidemic potential. Cell Host Microbe 15:706–16
    [Google Scholar]
  190. 190.  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]
  191. 191.  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 22:400–10
    [Google Scholar]
  192. 192.  Tao Y, Rotem A, Zhang H, Cockrell SK, Koehler SA et al. 2015. Artifact-free quantification and sequencing of rare recombinant viruses by using drop-based microfluidics. ChemBioChem 16:2167–71
    [Google Scholar]
  193. 193.  Tao Y, Rotem A, Zhang H, Chang CB, Basu A et al. 2015. Rapid, targeted and culture-free viral infectivity assay in drop-based microfluidics. Lab Chip 15:3934–40
    [Google Scholar]
  194. 194.  Guo F, Li S, Caglar MU, Mao Z, Liu W et al. 2017. Single-cell virology: on-chip investigation of viral infection dynamics. Cell Rep 21:1692–704
    [Google Scholar]
  195. 195.  Macosko EZ, Basu A, Satija R, Nemesh J, Shekhar K et al. 2015. Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell 161:1202–14
    [Google Scholar]
  196. 196.  Halpern KB, Shenhav R, Matcovitch-Natan O, Toth B, Lemze D et al. 2017. Single-cell spatial reconstruction reveals global division of labour in the mammalian liver. Nature 542:352–56
    [Google Scholar]
  197. 197.  Russell AB, Trapnell C, Bloom JD 2018. Extreme heterogeneity of influenza virus infection in single cells. eLife 7:e32303
    [Google Scholar]
  198. 198.  McKnight KL, Xie L, González-López O, Rivera-Serrano EE, Chen X, Lemon SM 2017. Protein composition of the hepatitis A virus quasi-envelope. PNAS 114:6587–92
    [Google Scholar]
  199. 199.  Lee CA, August A, Arnold JJ, Cameron CE 2016. Polymerase mechanism-based method of viral attenuation. Vaccine Technologies for Veterinary Viral Diseases: Methods and Protocols A Brun 83–104 New York, NY: Springer
    [Google Scholar]
  200. 200.  Naito T, Mori K, Ushirogawa H, Takizawa N, Nobusawa E et al. 2017. Generation of a genetically stable high-fidelity influenza vaccine strain. J. Virol. 91:e01073–16
    [Google Scholar]
/content/journals/10.1146/annurev-virology-101416-041718
Loading
/content/journals/10.1146/annurev-virology-101416-041718
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