Skip to main content

Getting to Know Viral Evolutionary Strategies: Towards the Next Generation of Quasispecies Models

  • Chapter
  • First Online:
Quasispecies: From Theory to Experimental Systems

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 392))

Abstract

Viral populations are formed by complex ensembles of genomes with broad phenotypic diversity. The adaptive strategies deployed by these ensembles are multiple and often cannot be predicted a priori. Our understanding of viral dynamics is mostly based on two kinds of empirical approaches: one directed towards characterizing molecular changes underlying fitness changes and another focused on population-level responses. Simultaneously, theoretical efforts are directed towards developing a formal picture of viral evolution by means of more realistic fitness landscapes and reliable population dynamics models. New technologies, chiefly the use of next-generation sequencing and related tools, are opening avenues connecting the molecular and the population levels. In the near future, we hope to be witnesses of an integration of these still decoupled approaches, leading into more accurate and realistic quasispecies models able to capture robust generalities and endowed with a satisfactory predictive power.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Acevedo A, Brodsky L, Andino R (2014) Mutational and fitness landscapes of an RNA virus revealed through population sequencing. Nature 505:686–690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agudo R, Arias A, Domingo E (2009) 5-fluorouracil in lethal mutagenesis of foot-and-mouth disease virus. Future Med Chem 1:529–539

    Article  CAS  PubMed  Google Scholar 

  • Agudo R, Ferrer-Orta C, Arias A, de la Higuera I, Perales C, Pérez-Luque R, Verdaguer N, Domingo E (2010) A multi-step process of viral adaptation to a mutagenic nucleoside analogue by modulation of transition types leads to extinction-escape. PLoS Pathog 6:e1001072

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aguirre J, Manrubia SC (2008) Effects of spatial competition on the diversity of a quasispecies. Phys Rev Lett 100:038106

    Article  PubMed  CAS  Google Scholar 

  • Arias A, Arnold JJ, Sierra M, Smidansky ED, Domingo E, Cameron CE (2008) Determinants of RNA-dependent RNA polymerase (in)fidelity revealed by kinetic analysis of the polymerase encoded by a foot-and-mouth disease virus mutant with reduced sensitivity to ribavirin. J Virol 82:12346–12355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arias A, Isabel de Ávila A, Sanz-Ramos M, Agudo R, Escarmís C, Domingo E (2013) Molecular dissection of a viral quasispecies under mutagenic treatment: positive correlation between fitness loss and mutational load. J Gen Virol 94:817–830

    Article  CAS  PubMed  Google Scholar 

  • Armstrong KL, Lee TH, Essex M (2011) Replicative fitness costs of nonnucleoside reverse transcriptase inhibitor drug resistance mutations on HIV subtype C. Antimicrob Agents Chemother 55:2146–2153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arribas M, Cabanillas L, Lázaro E (2011) Identification of mutations conferring 5-azacytidine resistance in bacteriophage Qβ. Virology 417:343–352

    Article  CAS  PubMed  Google Scholar 

  • Beerenwinkel N, Zagordi O (2011) Ultra-deep sequencing for the analysis of viral populations. Curr Opin Virol 1:1–6

    Article  CAS  Google Scholar 

  • Biebricher CK, Eigen M (2005) The error threshold. Virus Res 107:117-127

    Google Scholar 

  • Bonhoeffer S, Chappey C, Parkin NT, Whitcomb JM, Petropoulos CJ (2004) Evidence for positive epistasis in HIV-1. Science 306:1547–1550

    Article  CAS  PubMed  Google Scholar 

  • Borenstein E, Ruppin E (2006) Direct evolution of genetic robustness in microRNA. Proc Natl Acad Sci USA 103:6593–6598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buckheit RW Jr (2004) Understanding HIV resistance, fitness, replication capacity and compensation: targeting viral fitness as a therapeutic strategy. Expert Opin Investig Drugs 13:933–958

    Article  CAS  PubMed  Google Scholar 

  • Bull JJ, Badgett MR, Wichman HA (2000) Big-benefit mutations in a bacteriophage inhibited with heat. Mol Biol Evol 17:942–950

    Article  CAS  PubMed  Google Scholar 

  • Bull JJ, Sanjuán R, Wilke CO (2007) Theory of lethal mutagenesis for viruses. J Virol 81:2930–2939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burch CL, Chao L (2004) Epistasis and its relationship to canalization in the RNA virus phi 6. Genetics 167:559–567

    Google Scholar 

  • Carrasco P, de la Iglesia F, Elena SF (2007) Distribution of fitness and virulence effects caused by single-nucleotide substitutions in Tobacco Etch virus. J Virol 81:12979–12984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cases-González C, Arribas M, Domingo E, Lázaro E (2008) Beneficial effects of population bottlenecks in an RNA virus evolving at increased error rate. J Mol Biol 384:1119–1120

    Article  CAS  Google Scholar 

  • Chao L (1991) Levels of selection, evolution of sex in RNA viruses, and the origin of life. J Theor Biol 153:229–246

    Article  CAS  PubMed  Google Scholar 

  • Codoñer FM, Darós JA, Solé RV, Elena SF (2006) The fittest versus the flattest: experimental confirmation of the quasispecies effect with subviral pathogens. PLoS Pathog 2:e136

    Google Scholar 

  • Coffey LL, Beeharry Y, Bordería AV, Blanc H, Vignuzzi M (2011) Arbovirus high fidelity variant loses fitness in mosquitoes and mice. Proc Natl Acad Sci USA 108:16038--16043

    Google Scholar 

  • Coffey LL, Vignuzzi M (2011) Host alternation of chikungunya virus increases fitness while restricting population diversity and adaptability to novel selective pressures. J Virol 85:1025–1035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Covert AW, Lenski RE, Wilke CO, Ofria C (2013) Experiments on the role of deleterious mutations as stepping stones in adaptive evolution. Proc Natl Acad Sci USA 110:E3171–E3178

    Google Scholar 

  • Crotty S, Cameron CE, Andino R (2001) RNA virus error catastrophe: direct molecular test by using ribavirin. Proc Natl Acad Sci (USA) 98:6895–6900

    Article  CAS  Google Scholar 

  • Cuesta JA, Aguirre J, Capitán JA, Manrubia SC (2011) Struggle for space: viral extinction through competition for cells. Phys Rev Lett 106:028104

    Article  PubMed  CAS  Google Scholar 

  • Dapp MJ, Clouser CL, Patterson S, Mansky LM (2009) 5-Azacytidine can induce lethal mutagenesis in human immunodeficiency virus type 1. J Virol 83:11950–11958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das SR, Hensley SE, David A et al (2011) Fitness costs limit influenza A virus hemagglutinin glycosylation as an immune evasion strategy. Proc Natl Acad Sci (USA) 108:E1417–E1422

    Article  CAS  Google Scholar 

  • de Visser JAGM, Hermisson J, Wagner GP, Meyers LA, Bagheri HC, Blanchard JL, Chao L, Cheverud JM, Elena SF, Fontana W, Gibson G, Hansen TF, Krakauer D, Lewontin RC, Ofria C, Rice SH, von Dassow G, Wagner A, Whitlock MC (2003) Evolution and detection of genetic robustness. Evolution 57:1959–1972

    PubMed  Google Scholar 

  • Domingo E, Sheldon J, Perales C (2012) Viral quasispecies evolution. Microbiol Mol Biol Rev 76:159–216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Domingo E, González-Lopez C, Pariente N, Airaksinen A, Escarmís C (2005) Population dynamics of RNA viruses: the essential contribution of mutant spectra. In: Peters CJ, Calisher CH (eds) Infectious diseases from nature: mechanisms of viral emergence and persistence, pp 59–71

    Google Scholar 

  • Domingo-Calap P, Cuevas JM, Sanjuán R (2009) The fitness effects of random mutations in single-stranded DNA and RNA bacteriophages. PLoS Genet 5:e1000742

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Drake JW, Holland JJ (1999) Mutation rates among RNA viruses. Proc Natl Acad Sci (USA) 96:13910–13913

    Article  CAS  Google Scholar 

  • Eigen M (1971) Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften 58:465–523

    Article  CAS  PubMed  Google Scholar 

  • Eigen M (2002) Error catastrophe and antiviral strategy. Proc Natl Acad Sci U S A 99:13374–13376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elena SF (1999) Little evidence for synergism among deleterious mutations in a nonsegmented RNA virus. J Mol Evol 49:703–707

    Article  CAS  PubMed  Google Scholar 

  • Escarmís C, Gómez-Mariano G, Dávila M, Lázaro E, Domingo E (2002) Resistance to extinction of low fitness virus subjected to plaque-to-plaque transfers: diversification by mutation clustering. J Mol Biol 315:647–661

    Article  PubMed  CAS  Google Scholar 

  • Gago S, Elena SF, Flores R, Sanjuán R (2009) Extremely high mutation rate of a hammerhead viroid. Science 323:1308

    Article  CAS  PubMed  Google Scholar 

  • García-Arriaza J, Manrubia SC, Toja M, Domingo E, Escarmís C (2004) Evolutionary transition toward defective RNAs that are infectious by complementation. J Virol 78:11678–11685

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Good BH, Rouzine IM, Balick DJ, Hallatschek O, Desai MM (2012) Distribution of fixed beneficial mutations and the rate of adaptation in asexual populations. Proc Natl Acad Sci USA 109:4950–4955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graci JD, Gnädig NF, Galarraga JE, Castro C, Vignuzzi M, Cameron CE (2012) Mutational robustness of an RNA virus influences sensitivity to lethal mutagenesis. J Virol 86:2869–2873

    Google Scholar 

  • Grande-Pérez A, Sierra S, Castro MG, Domingo E, Lowenstein PR (2002) Molecular indetermination in the transition to error catastrophe: systematic elimination of lymphocytic choriomeningitis virus through mutagenesis does not correlate linearly with large increases in mutant spectrum complexity. Proc Natl Acad Sci (USA) 99:12938–12943

    Article  CAS  Google Scholar 

  • Grande-Pérez A, Lázaro E, Lowenstein P, Domingo E, Manrubia SC (2005) Suppression of viral infectivity through lethal defection. Proc Natl Acad Sci U S A 102:4448–4452

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Harris RS, Bishop KN, Sheehy AM, Craig HM, Petersen-Mahrt SK et al (2003) DNA deamination mediates innate immunity to retroviral infection. Cell 113:803–809

    Article  CAS  PubMed  Google Scholar 

  • Holland J, Spindler K, Horodyski F, Grabau E, Nichol S, VandePol S (1982) Rapid evolution of RNA genomes. Science 215:1577–1585

    Article  CAS  PubMed  Google Scholar 

  • Holland JJ, Domingo E, de la Torre JC, Steinhauer DA (1990) Mutation frequencies at defined single codon sites in vesicular stomatitis virus can be increased only slightly by chemical mutagenesis. J Virol 64:3960–3962

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holmes EC (2003) Error thresholds and the constraints to RNA virus evolution. Trends Microbiol 11:543–546

    Article  CAS  PubMed  Google Scholar 

  • Holtz CM, Mansky LM (2013) Variation of HIV-1 mutation spectra among cell types. J Virol 87:5296–5299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hull R (2013) Plant virology. Academic Press, p 1120

    Google Scholar 

  • Huynen MA, Stadler PF, Fontana W (1996) Smoothness within ruggedness: The role of neutrality in adaptation. Proc Natl Acad Sci USA 93:397–401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iranzo J, Manrubia SC (2009) Stochastic extinction of viral infectivity through the action of defectors. Europhys Lett 85:18001

    Article  CAS  Google Scholar 

  • Iranzo J, Manrubia SC (2012) Evolutionary dynamics of genome segmentation in multipartite viruses. Proc R Soc Lond B 279:3812–3819

    Article  Google Scholar 

  • Iranzo J, Perales C, Domingo E, Manrubia S (2011) Tempo and mode of inhibitor-mutagen antiviral therapies: A multidisciplinary approach. Proc Natl Acad Sci USA 108:16008–16013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Julias JG, Pathak VK (1998) Deoxyribonucleoside triphosphate pool imbalances in vivo are associated with an increased retroviral mutation rate. J Virol 72:7941–7949

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kimura M, Maruyama T (1966) The mutational load with epistatic interactions in fitness. Genetics 54:1337–1351

    CAS  PubMed  PubMed Central  Google Scholar 

  • Koelle K, Cobey S, Grenfell B, Pascual M (2006) Epochal evolution shapes the phylodynamics of interpandemic influenza A (H3N2) in humans. Science 314:1898–1903

    Article  CAS  PubMed  Google Scholar 

  • Kouyos RD, Leventhal GE, Hinkley T, Haddad M, Whitcomb JM, Petropoulos CJ, Bonhoeffer S (2012) Exploring the complexity of the HIV-1 fitness landscape. PLoS Genet 8:e1002551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lalić J, Elena SF (2012) Magnitude and sign epistasis among deleterious mutations in a positive-sense plant RNA virus. Heredity 109:71–77

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lalić J, Elena SF (2013) Epistasis between mutations is host-dependent for an RNA virus. Biol Lett 9:20120396

    Article  PubMed  PubMed Central  Google Scholar 

  • Lauring AS1, Frydman J, Andino R (2013) The role of mutational robustness in RNA virus evolution. Nat Rev Microbiol 11:327–336

    Google Scholar 

  • Lázaro E, Escarmís C, Domingo E, Manrubia SC (2002) Modeling viral genome fitness evolution associated with serial bottleneck events: evidence of stationary states of fitness. J Virol 76:8675–8681

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lázaro E, Escarmís C, Pérez-Mercader J, Manrubia SC, Domingo E (2003) Resistance of virus to extinction on bottleneck passages: study of a decaying and fluctuating pattern of fitness loss. Proc Natl Acad Sci USA 100:10830–10835

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lázaro E, Escarmís C, Manrubia SC (2006) Population bottlenecks in quasispecies dynamics. Curr Top Microbiol Immunol 299:141–170

    PubMed  Google Scholar 

  • Lee CH, Gilbertson DL, Novella IS, Huerta R, Domingo E, Holland JJ (1997) Negative effects of chemical mutagenesis on the adaptive behavior of vesicular stomatitis virus. J Virol 71:3636–3640

    CAS  PubMed  PubMed Central  Google Scholar 

  • Loeb LA, Essigmann JM, Kazazi F, Zhang J, Rose KD, Mullins JI (1999) Lethal mutagenesis of HIV with mutagenic nucleoside analogs. Proc Natl Acad Sci USA 96:1492–1497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lourenço J, Galtier N, Glémin S (2011) Complexity, pleiotropy, and the fitness effect of mutations. Evolution 65:1559–1571

    Article  PubMed  Google Scholar 

  • Manrubia SC, Domingo E, Lázaro E (2010) Pathways to extinction: Beyond the error threshold. Phil Trans R Soc London B 365:1943–1952

    Article  Google Scholar 

  • Manrubia SC, Lázaro E (2006) Viral evolution. Phys Life Revs 3:65–92

    Article  Google Scholar 

  • Manrubia SC (2012) Modelling viral evolution and adaptation: challenges and rewards. Curr Opin Virol 2:531–537

    Article  CAS  PubMed  Google Scholar 

  • Martínez JP, Bocharov G, Ignatovich A, Reiter J, Dittmar MT, Wain-Hobson S, Meyerhans A (2011) Fitness ranking of individual mutants drives patterns of epistatic interactions in HIV-1. PLoS ONE 6:e18375

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maynard Smith J (1970) Natural Selection and the concept of a protein space. Nature 225:563–564

    Article  Google Scholar 

  • Moreno H, Tejero H, de la Torre JC, Domingo E, Martín V (2012) Mutagenesis-mediated virus extinction: virus-dependent effect of viral load on sensitivity to lethal defection. PLoS ONE 7:e32550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moreno E, Ojosnegros S, García-Arriaza J, Escarmís C, Domingo E, Perales C (2014) Exploration of sequence space as the basis of viral RNA genome segmentation. Proc Natl Acad Sci USA 111:6678–6683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muller HJ (1964) The relation of recombination to mutational advance. Mutat Res 1:2–9

    Article  Google Scholar 

  • Nee S (1987) The evolution of multicompartmental genomes in viruses. J Mol Evol 25:277–281

    Article  CAS  PubMed  Google Scholar 

  • Núñez JI, Molina N, Baranowski E, Domingo E, Clark S, Burman A, Berryman S, Jackson T, Sobrino F (2007) Guinea pig-adapted foot-and-mouth disease virus with altered receptor recognition can productively infect a natural host. J Virol 81:8497–8506

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ojosnegros S, Agudo R, Sierra M, Briones C, Sierra S, González-López C, Domingo E, Cristina J (2008) Topology of evolving, mutagenized viral populations: quasispecies expansion, compression, and operation of negative selection. BMC Evol Biol 8:207

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ojosnegros S, García-Arriaza J, Escarmís C, Manrubia SC, Perales C, Arias A, García Mateu M, Domingo E (2011) Viral genome segmentation can result from a trade-off between genetic content and particle stability. PLoS Genet 7:e1001344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orr HA (1998) The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52:935–949

    Article  Google Scholar 

  • Orr HA (2003) The distribution of fitness effects among beneficial mutations. Genetics 163:1519–1526

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pariente N, Airaksinen A, Domingo E (2003) Mutagenesis versus inhibition in the efficiency of extinction of foot-and-mouth disease virus. J Virol 77:7131–7138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perales C, Mateo R, Mateu MG, Domingo E (2007) Insights into RNA virus mutant spectrum and lethal mutagenesis events: replicative interference and complementation by multiple point mutants. J Mol Biol 369:985–1000

    Article  CAS  PubMed  Google Scholar 

  • Perales C, Agudo R, Manrubia SC, Domingo E (2011a) Influence of mutagenesis and viral load on the sustained low-level replication of an RNA virus. J Mol Biol 407:60–78

    Article  CAS  PubMed  Google Scholar 

  • Perales C, Martín V, Domingo E (2011b) Lethal mutagenesis of viruses. Curr Opin Virol 1:419–422

    Article  CAS  PubMed  Google Scholar 

  • Perales C, Henry M, Domingo E, Wain-Hobson S, Vartanian JP (2011c) Lethal mutagenesis of foot-and-mouth disease virus involves shifts in sequence space. J Virol 85:12227–12240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perales C, Iranzo J, Manrubia SC, Domingo E (2012) The impact of quasispecies dynamics on the use of therapeutics. Trends Microbiol 20:595–603

    Article  CAS  PubMed  Google Scholar 

  • Pfeiffer JK, Kierkegaard K (2003) A single mutation in poliovirus RNA-dependent RNA polymerase confers resistance to mutagenic nucleotide analogs via increased fidelity. Proc Natl Acad Sci USA 100:7289–7294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfeiffer JK, Kierkegaard K (2005) Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice. PLoS Pathog 1:e11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Phillips PC (2008) Epistasis—the essential role of gene interactions in the structure and evolution of genetic systems. Nat Rev Genet 9:855–867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pita JS, de Miranda JR, Schneider WL, Roossinck MJ (2007) Environment determines fidelity for an RNA virus replicase. J Virol 81:9072–9077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poelwijk FJ, Kiviet DJ, Weinreich DM, Tans SJ (2007) Empirical fitness landscapes reveal accessible evolutionary paths. Nature 445:383–386

    Google Scholar 

  • Poelwijk FJ, Tănase-Nicola S, Kiviet DJ, Tans SJ (2011) Reciprocal sign epistasis is a necessary condition for multi-peaked fitness landscapes. J Theor Biol 272:141–144

    Article  PubMed  Google Scholar 

  • Radford AD, Chapman D, Dixon L, Chantrey J, Darby AC, Hall N (2012) Application of next-generation sequencing technologies in virology. J Gen Virol 93:1853–1868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Remold SK, Rambaut A, Turner PE (2008) Evolutionary genomics of host adaptation in vesicular stomatitis virus. Mol Biol Evol 25:1138–1147

    Article  CAS  PubMed  Google Scholar 

  • Rokyta DR, Joyce P, Caudle SB, Miller C, Beisel CJ, Wichman HA (2011) Epistasis between beneficial mutations and the phenotype-to-fitness map for a ssDNA virus. PLoS Genet 7(6):e1002075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saakian DB, Hu C-K (2006) Exact solution of the Eigen model with general fitness functions and degradation rates. Proc Natl Acad Sci USA 103:4935–4939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saakian DB, Muñoz E, Hu C-K, Deem MW (2006) Quasispecies theory for multiple-peak fitness landscapes. Phys Rev E 73:041913

    Article  CAS  Google Scholar 

  • Sierra S, Dávila M, Lowenstein PR, Domingo E (2000) Response of foot-and-mouth disease virus to increased mutagenesis: influence of viral load and fitness in loss of infectivity. J Virol 74:8316–8323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sánchez-Navarro JA, Zwart MP, Elena SF (2013) Effects of the number of genome segments on primary and systemic infections with a multipartite plant RNA virus. J Virol 87:10805–10815

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sanjuán R, Moya A, Elena SF (2004a) The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. Proc Natl Acad Sci USA 101:8396–8401

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanjuán R, Moya A, Elena SF (2004b) The contribution of epistasis to the architecture of fitness in an RNA virus. Proc Natl Acad Sci USA 101:15376–15379

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sanjuán R, Cuevas JM, Furió V, Holmes EC, Moya A (2007) Selection for robustness in mutagenized RNA viruses. PLoS Genet 3:e93

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sanjuán R (2010) Mutational fitness effects in RNA and single-stranded DNA viruses: common patterns revealed by site-directed mutagenesis studies. Phil Trans R Soc Lond B 365:1975–1982

    Article  CAS  Google Scholar 

  • Sanjuán R, Nebot MR, Chirico N, Mansky LM, Belshaw R (2010) Viral mutation rates. J Virol 84:9733–9748

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Seronello S, Montanez J, Presleigh K, Barlow M, Park SB et al (2011) Ethanol and reactive species increase basal sequence heterogeneity of hepatitis C virus and produce variants with reduced susceptibility to antivirals. PLoS ONE 6:e27436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Severson WE, Schmaljohn CS, Javadian A, Jonsson CB (2003) Ribavirin causes error catastrophe during Hantaan virus replication. J Virol 77:481–488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sicard A, Yvon M, Timchenko T, Gronenborn B, Michalakis Y et al (2013) Gene copy number is differentially regulated in a multipartite virus. Nat Commun 4:2248

    Article  PubMed  CAS  Google Scholar 

  • Szendro IG, Schenk MF, Franke J, Krug J, de Visser AGM (2013) Quantitative analyses of empirical fitness landscapes. J Stat Mech P01005

    Google Scholar 

  • Takeuchi N, Hogeweg P (2007) Error-threshold exists in fitness landscapes with lethal mutants. BMC Evol Biol 7:15

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsetsarkin KA, McGee CE, Volk SM, Vanlandingham DL, Weaver SC, Higgs S (2009) Epistatic roles of E2 glycoprotein mutations in adaption of chikungunya virus to Aedes albopictus and Ae. aegypti mosquitoes. PLoS ONE 4:e6835

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Turner PE, Elena SF (2000) Cost of host radiation in an RNA virus. Genetics 156:1465–1470

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vasilakis N, Deardorff ER, Kenney JL, Rossi SL, Hanley KA, Weaver SC (2009) Mosquitoes put the brake on arbovirus evolution: experimental evolution reveals slower mutation accumulation in mosquito than vertebrate cells. PLoS Pathog 5:e1000467

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R (2006) Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 39:344–348

    Article  CAS  Google Scholar 

  • Wagner A (2011) The origins of evolutionary innovations. Oxford University Press, Oxford

    Google Scholar 

  • Wagner A (2012) The role of robustness in phenotypic adaptation and innovation. Proc R Soc Lond B 279:1249–1258

    Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Withlock MC, Phillips PC, Moore FBG, Tonsor SJ (1995) Multiple fitness peaks and epistasis. Annu Rev Ecol Evol Syst 26:601–629

    Article  Google Scholar 

  • Woo HJ, Reifman J (2012) A quantitative quasispecies theory-based model of virus escape mutation under immune selection. Proc Natl Acad Sci USA 109:12980–12985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wright S (1931) Evolution in mendelian populations. Genetics 16:97–159

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors acknowledge support of the Spanish MINECO through projects BFU2013-41329, FIS2011-27569, and FIS2014-57686.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Susanna Manrubia .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Manrubia, S., Lázaro, E. (2015). Getting to Know Viral Evolutionary Strategies: Towards the Next Generation of Quasispecies Models. In: Domingo, E., Schuster, P. (eds) Quasispecies: From Theory to Experimental Systems. Current Topics in Microbiology and Immunology, vol 392. Springer, Cham. https://doi.org/10.1007/82_2015_457

Download citation

Publish with us

Policies and ethics