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Evaluating the Evolutionary Dynamics of Viral Populations

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Abstract

Phylodynamic techniques combine epidemiological and genetic information to analyze the evolutionary and spatiotemporal dynamics of rapidly evolving pathogens, such as influenza A or human immunodeficiency viruses. We introduce allele dynamics plots (AD-plots) as a method for visualizing the evolutionary dynamics of a gene in a population. Using AD-plots, we propose to identify the alleles that are likely to be subject to directional selection. We analyze the method’s merits with a detailed study of the evolutionary dynamics of seasonal influenza A viruses. AD-plots for the major surface protein of seasonal influenza A (H3N2) and the 2009 swine-origin influenza A (H1N1) viruses show the succession of substitutions that became fixed in the evolution of the two viral populations. They also allow the early identification of those viral strains that later rise to predominance, which is important for the problem of vaccine strain selection. In summary, we describe a technique that reveals the evolutionary dynamics of a rapidly evolving population and allows us to identify alleles and associated genetic changes that might be under directional selection. The method can be applied for the study of influenza A viruses and other rapidly evolving species or viruses.

Adapted from: Steinbrück L, McHardy AC (2011) Allele dynamics plots for the study of evolutionary dynamics in viral populations. Nucleic Acids Res 39(1):e4, by permission of Oxford University Press.

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References

  1. Grenfell BT, Pybus OG, Gog JR, Wood JLN, Daly JM, Mumford JA, Holmes EC (2004) Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303:327–332

    Article  PubMed  CAS  Google Scholar 

  2. Pybus OG, Rambaut A (2009) Evolutionary analysis of the dynamics of viral infectious disease. Nat Rev Genet 10:540–550

    Article  PubMed  CAS  Google Scholar 

  3. Wallace RG, HoDac HM, Lathrop RH, Fitch WM (2007) A statistical phylogeography of influenza A H5N1. Proc Natl Acad Sci U S A 104:4473–4478

    Article  PubMed  CAS  Google Scholar 

  4. Keele BF, Van Heuverswyn F, Li Y, Bailes E, Takehisa J, Santiago ML, Bibollet-Ruche F, Chen Y, Wain LV, Liegeois F et al (2006) Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313:523–526

    Article  PubMed  CAS  Google Scholar 

  5. Lemey P, Pybus OG, Wang B, Saksena NK, Salemi M, Vandamme A-M (2003) Tracing the origin and history of the HIV-2 epidemic. Proc Natl Acad Sci U S A 100:6588–6592

    Article  PubMed  CAS  Google Scholar 

  6. Bush R (1999) Positive selection on the H3 hemagglutinin gene of human influenza virus A. Mol Biol Evol 16:1457–1465

    Article  PubMed  CAS  Google Scholar 

  7. Kryazhimskiy S, Plotkin JB (2008) The population genetics of dN/dS. PLoS Genet 4:e1000304

    Article  PubMed  Google Scholar 

  8. Pond SLK, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679

    Article  PubMed  CAS  Google Scholar 

  9. Pond K, Sergei L, Poon AFY, Brown L, Andrew J, Frost SDW (2008) A maximum likelihood method for detecting directional evolution in protein sequences and its application to influenza A virus. Mol Biol Evol 25:1809–1824

    Article  CAS  Google Scholar 

  10. Ricklefs RE (2007) Estimating diversification rates from phylogenetic information. Trends Ecol Evol 22:601–610

    Article  PubMed  Google Scholar 

  11. 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  PubMed  CAS  Google Scholar 

  12. Fouchier RAM, Munster V, Wallensten A, Bestebroer TM, Herfst S, Smith D, Rimmelzwaan GF, Olsen B, Osterhaus ADME (2005) Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol 79:2814–2822

    Article  PubMed  CAS  Google Scholar 

  13. WHO (2009) Recommended composition of influenza virus vaccines for use in 2009–2010 influenza season (northern hemisphere winter). Wkly Epidemiol Rec 84:65–72

    Google Scholar 

  14. WHO (2010) Recommended viruses for influenza vaccines for use in the 2010–2011 northern hemisphere influenza season. Wkly Epidemiol Rec 85:81–92

    Google Scholar 

  15. Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF, Osterhaus ADME, Fouchier RAM (2004) Mapping the antigenic and genetic evolution of influenza virus. Science 305:371–376

    Article  PubMed  CAS  Google Scholar 

  16. Wiley D, Wilson I, Skehel J (1981) Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 289:373–378

    Article  PubMed  CAS  Google Scholar 

  17. Wiley DC, Skehel JJ (1987) The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu Rev Biochem 56:365–394

    Article  PubMed  CAS  Google Scholar 

  18. Wilson IA, Cox NJ (1990) Structural basis of immune recognition of influenza virus hemagglutinin. Annu Rev Immunol 8:737–771

    Article  PubMed  CAS  Google Scholar 

  19. Skehel JJ, Wiley DC (2000) Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 69:531–569

    Article  PubMed  CAS  Google Scholar 

  20. Kuiken T, Holmes EC, McCauley J, Rimmelzwaan GF, Williams CS, Grenfell BT (2006) Host species barriers to influenza virus infections. Science 312:394–397

    Article  PubMed  CAS  Google Scholar 

  21. Webster R, Bean W, Gorman O, Chambers T, Kawaoka Y (1992) Evolution and ecology of influenza A viruses. Microbiol Rev 56:152–179

    PubMed  CAS  Google Scholar 

  22. Lowen AC, Palese P (2007) Influenza virus transmission: basic science and implications for the use of antiviral drugs during a pandemic. Infect Disord Drug Targets 7:318–328

    Article  PubMed  CAS  Google Scholar 

  23. Morens DM, Taubenberger JK, Fauci AS (2009) The persistent legacy of the 1918 influenza virus. N Engl J Med 361:225–229

    Article  PubMed  CAS  Google Scholar 

  24. Neumann G, Noda T, Kawaoka Y (2009) Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459:931–939

    Article  PubMed  CAS  Google Scholar 

  25. Zimmer SM, Burke DS (2009) Historical perspective – emergence of influenza A (H1N1) viruses. N Engl J Med 361:279–285

    Article  PubMed  CAS  Google Scholar 

  26. Cox NJ, Brammer TL, Regnery HL (1994) Influenza: global surveillance for epidemic and pandemic variants. Eur J Epidemiol 10:467–470

    Article  PubMed  CAS  Google Scholar 

  27. Russell CA, Jones TC, Barr IG, Cox NJ, Garten RJ, Gregory V, Gust ID, Hampson AW, Hay AJ, Hurt AC et al (2008) Influenza vaccine strain selection and recent studies on the global migration of seasonal influenza viruses. Vaccine 26:31–34

    Article  Google Scholar 

  28. Nelson MI, Simonsen L, Viboud C, Miller MA, Holmes EC, Levin B (2007) Phylogenetic analysis reveals the global migration of seasonal influenza A viruses. PLoS Pathog 3:e131

    Article  Google Scholar 

  29. Russell CA, Jones TC, Barr IG, Cox NJ, Garten RJ, Gregory V, Gust ID, Hampson AW, Hay AJ, Hurt AC et al (2008) The global circulation of seasonal influenza A (H3N2) viruses. Science 320:340–346

    Article  PubMed  CAS  Google Scholar 

  30. Rambaut A, Pybus OG, Nelson MI, Viboud C, Taubenberger JK, Holmes EC (2008) The genomic and epidemiological dynamics of human influenza A virus. Nature 453:615–619

    Article  PubMed  CAS  Google Scholar 

  31. Shih ACC, Hsiao TC, Ho MS, Li WH (2007) Simultaneous amino acid substitutions at antigenic sites drive influenza A hemagglutinin evolution. Proc Natl Acad Sci U S A 104:6283–6288

    Article  PubMed  CAS  Google Scholar 

  32. Plotkin JB, Dushoff J, Levin SA (2002) Hemagglutinin sequence clusters and the antigenic evolution of influenza A virus. Proc Natl Acad Sci U S A 99:6263–6268

    Article  PubMed  CAS  Google Scholar 

  33. Du X, Wang Z, Wu A, Song L, Cao Y, Hang H, Jiang T (2008) Networks of genomic co-occurrence capture characteristics of human influenza A (H3N2) evolution. Genome Res 18:178–187

    Article  PubMed  CAS  Google Scholar 

  34. Xia Z, Jin G, Zhu J, Zhou R (2009) Using a mutual information-based site transition network to map the genetic evolution of influenza A/H3N2 virus. Bioinformatics 25:2309–2317

    Article  PubMed  CAS  Google Scholar 

  35. Bush RM, Bender CA, Subbarao K, Cox NJ, Fitch WM (1999) Predicting the evolution of human influenza A. Science 286:1921–1925

    Article  PubMed  CAS  Google Scholar 

  36. Nozawa M, Suzuki Y, Nei M (2009) Reliabilities of identifying positive selection by the branch-site and the site-prediction methods. Proc Natl Acad Sci U S A 106:6700–6705

    Article  PubMed  CAS  Google Scholar 

  37. Fouchier RAM, Smith DJ (2010) Use of antigenic cartography in vaccine seed strain selection. Avian Dis 54:220–223

    Article  PubMed  Google Scholar 

  38. Huang JW, King CC, Yang JM (2009) Co-evolution positions and rules for antigenic variants of human influenza A/H3N2 viruses. BMC Bioinformatics 10:S41

    Article  PubMed  Google Scholar 

  39. Lee MS, Chen MC, Liao YC, Hsiung CA (2007) Identifying potential immunodominant positions and predicting antigenic variants of influenza A/H3N2 viruses. Vaccine 25:8133–8139

    Article  PubMed  CAS  Google Scholar 

  40. Liao YC, Lee MS, Ko CY, Hsiung CA (2008) Bioinformatics models for predicting antigenic variants of influenza A/H3N2 virus. Bioinformatics 24:505–512

    Article  PubMed  CAS  Google Scholar 

  41. Bao Y, Bolotov P, Dernovoy D, Kiryutin B, Zaslavsky L, Tatusova T, Ostell J, Lipman D (2008) The influenza virus resource at the National Center for Biotechnology Information. J Virol 82:596–601

    Article  PubMed  CAS  Google Scholar 

  42. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113

    Article  PubMed  Google Scholar 

  43. Guindon S, Gascuel O (2003) A simple, fast, and accurate method to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  44. Zwickl D (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Thesis, The University of Texas at Austin

    Google Scholar 

  45. Futuyma DJ (1998) Evolutionary biology, 3rd edn. Sinauer Associates, Sunderland, MA

    Google Scholar 

  46. Hein J, Schierup M, Wiuf C (2005) Gene genealogies, variation and evolution: a primer in coalescent theory. Oxford University Press, USA

    Google Scholar 

  47. Templeton AR (2006) Population genetics and microevolutionary theory. Wiley, Hoboken, NJ

    Book  Google Scholar 

  48. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  49. Drummond A, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  PubMed  Google Scholar 

  50. Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416

    Article  Google Scholar 

  51. Felsenstein J (2004) Inferring phylogenies. Sinauer Associates, Sunderland, MA

    Google Scholar 

  52. Pagel M, Meade A, Barker D (2004) Bayesian estimation of ancestral character states on phylogenies. Syst Biol 53:673–684

    Article  PubMed  Google Scholar 

  53. Nelson MI, Holmes EC (2007) The evolution of epidemic influenza. Nat Rev Genet 8:196–205

    Article  PubMed  CAS  Google Scholar 

  54. Ghedin E, Sengamalay NA, Shumway M, Zaborsky J, Feldblyum T, Subbu V, Spiro DJ, Sitz J, Koo H, Bolotov P et al (2005) Large-scale sequencing of human influenza reveals the dynamic nature of viral genome evolution. Nature 437:1162–1166

    Article  PubMed  CAS  Google Scholar 

  55. WHO (1999) Recommended composition of influenza virus vaccines for use in the 2000 influenza season. Wkly Epidemiol Rec 74:321–325

    Google Scholar 

  56. WHO (2000) Recommended composition of influenza virus vaccines for use in the 2000–2001 season. Wkly Epidemiol Rec 75:61–65

    Google Scholar 

  57. WHO (2001) Recommended composition of influenza virus vaccines for use in the 2001–2002 influenza season. Wkly Epidemiol Rec 76:58–61

    Google Scholar 

  58. WHO (2002) Recommended composition of influenza virus vaccines for use in the 2002–2003 influenza season. Wkly Epidemiol Rec 77:62–66

    Google Scholar 

  59. Lin Y, Gregory V, Bennett M, Hay A (2004) Recent changes among human influenza viruses. Virus Res 103:47–52

    Article  PubMed  CAS  Google Scholar 

  60. Hay AJ, Lin YP, Gregory V, Bennet M (2003) WHO collaborating centre for reference and research on influenza, annual report. National Institute for Medical Research, London

    Google Scholar 

  61. Hay AJ, Lin YP, Gregory V, Bennet M (2005) WHO collaborating centre for reference and research on influenza, interim report February. National Institute for Medical Research, London

    Google Scholar 

  62. Hay AJ, Lin YP, Gregory V, Bennet M (2006) WHO collaborating centre for reference and research on influenza, interim report March. National Institute for Medical Research, London

    Google Scholar 

  63. Hay AJ, Daniels R, Lin YP, Xiang Z, Gregory V, Bennet M, Whittaker L (2007) WHO collaborating centre for reference and research on influenza, interim report September. National Institute for Medical Research, London

    Google Scholar 

  64. WHO (2000) Recommended composition of influenza virus vaccines for use in the 2001 influenza season. Wkly Epidemiol Rec 75:330–333

    Google Scholar 

  65. WHO (2001) Recommended composition of influenza virus vaccines for use in the 2002 influenza season. Wkly Epidemiol Rec 76:311–314

    Google Scholar 

  66. WHO (2002) Recommended composition of influenza virus vaccines for use in the 2003 influenza season. Wkly Epidemiol Rec 77:344–348

    Google Scholar 

  67. WHO (2003) Recommended composition of influenza virus vaccines for use in the 2003–2004 influenza season. Wkly Epidemiol Rec 78:58–62

    Google Scholar 

  68. WHO (2003) Recommended composition of influenza virus vaccines for use in the 2004 influenza season. Wkly Epidemiol Rec 78:375–379

    Google Scholar 

  69. WHO (2004) Recommended composition of influenza virus vaccines for use in the 2004–2005 influenza season. Wkly Epidemiol Rec 79:88–92

    Google Scholar 

  70. WHO (2004) Recommended composition of influenza virus vaccines for use in the 2005 influenza season. Wkly Epidemiol Rec 79:369–373

    Google Scholar 

  71. WHO (2005) Recommended composition of influenza virus vaccines for use in the 2005–2006 influenza season. Wkly Epidemiol Rec 80:66–71

    Google Scholar 

  72. Jin H, Zhou H, Liu H, Chan W, Adhikary L, Mahmood K, Lee MS, Kemble G (2005) Two residues in the hemagglutinin of A/Fujian/411/02-like influenza viruses are responsible for antigenic drift from A/Panama/2007/99. Virology 336:113–119

    Article  PubMed  CAS  Google Scholar 

  73. WHO (2005) Recommended composition of influenza virus vaccines for use in the 2006 influenza season. Wkly Epidemiol Rec 80:342–347

    Google Scholar 

  74. WHO (2006) Recommended composition of influenza virus vaccines for use in the 2007 influenza season. Wkly Epidemiol Rec 81:390–395

    Google Scholar 

  75. WHO (2007) Recommended composition of influenza virus vaccines for use in the 2007–2008 influenza season. Wkly Epidemiol Rec 82:69–74

    Google Scholar 

  76. WHO (2006) Recommended composition of influenza virus vaccines for use in the 2006–2007 influenza season. Wkly Epidemiol Rec 81:82–86

    Google Scholar 

  77. WHO (2007) Recommended composition of influenza virus vaccines for use in the 2008 influenza season. Wkly Epidemiol Rec 82:351–356

    Google Scholar 

  78. WHO (2008) Recommended composition of influenza virus vaccines for use in the 2008–2009 influenza season. Wkly Epidemiol Rec 83:81–87

    Google Scholar 

  79. WHO (2008) Recommended composition of influenza virus vaccines for use in the 2009 southern hemisphere influenza season. Wkly Epidemiol Rec 83:366–372

    Google Scholar 

  80. WHO (1999) Recommended composition of influenza virus vaccines for use in the 1999–2000 season. Wkly Epidemiol Rec 74:57–61

    Google Scholar 

  81. Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, Balish A, Sessions WM, Xu X, Skepner E, Deyde V et al (2009) Antigenic and genetic characteristics of swine-origin 2009 A (H1N1) influenza viruses circulating in humans. Science 325:197–201

    Article  PubMed  CAS  Google Scholar 

  82. Smith G, Vijaykrishna D, Bahl J, Lycett S, Worobey M, Pybus O, Ma S, Cheung C, Raghwani J, Bhatt S et al (2009) Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459:1122–1125

    Article  PubMed  CAS  Google Scholar 

  83. A Novel Swine-Origin Influenza (H1N1) Virus Investigation Team (2009) Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med 360:2605–2615

    Article  Google Scholar 

  84. Fereidouni SR, Beer M, Vahlenkamp T, Starick E (2009) Differentiation of two distinct clusters among currently circulating influenza A (H1N1)v viruses, March–September 2009. Euro Surveill 14:19409–19411

    PubMed  Google Scholar 

  85. Pan C, Cheung B, Tan S, Li C, Li L, Liu S, Jiang S (2010) Genomic signature and mutation trend analysis of pandemic (H1N1) 2009 influenza A virus. PLoS One 5:e9549

    Article  PubMed  Google Scholar 

  86. Nobusawa E, Aoyama T, Kato H, Suzuki Y, Tateno Y, Nakajima K (1991) Comparison of complete amino acid sequences and receptor-binding properties among 13 serotypes of hemagglutinins of influenza A viruses. Virology 182:475–485

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Alice Carolyn McHardy .

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Steinbrück, L., McHardy, A.C. (2013). Evaluating the Evolutionary Dynamics of Viral Populations. In: Sree Hari Rao, V., Durvasula, R. (eds) Dynamic Models of Infectious Diseases. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-9224-5_8

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