The emergence and reemergence of rapidly evolving RNA viruses—particularly those responsible for respiratory diseases, such as influenza viruses and coronaviruses—pose a significant threat to global health, including the potential of major pandemics. Importantly, recent advances in high-throughput genome sequencing enable researchers to reveal the genomic diversity of these viral pathogens at much lower cost and with much greater precision than they could before. In particular, the genome sequence data generated allow inferences to be made on the molecular basis of viral emergence, evolution, and spread in human populations in real time. In this review, we introduce recent computational methods that analyze viral genomic data, particularly in combination with metadata such as sampling time, geographic location, and virulence. We then outline the insights these analyses have provided into the fundamental patterns and processes of evolution and emergence in human respiratory RNA viruses, as well as the major challenges in such genomic analyses.


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Literature Cited

  1. Agoti CN, Mayieka LM, Otieno JR, Ahmed JA, Fields BS. 1.  et al. 2014. Examining strain diversity and phylogeography in relation to an unusual epidemic pattern of respiratory syncytial virus (RSV) in a long-term refugee camp in Kenya. BMC Infect. Dis. 14:178 [Google Scholar]
  2. Agoti CN, Otieno JR, Munywoki PK, Mwihuri AG, Cane PA. 2.  et al. 2015. Local evolutionary patterns of human respiratory syncytial virus derived from whole-genome sequencing. J. Virol. 89:3444–54 [Google Scholar]
  3. Ali A, Daniels JB, Zhang Y, Rodriguez-Palacios A, Hayes-Ozello K. 3.  et al. 2011. Pandemic and seasonal human influenza virus infections in domestic cats: prevalence, association with respiratory disease, and seasonality patterns. J. Clin. Microbiol. 49:4101–5 [Google Scholar]
  4. Azhar EI, El-Kafrawy SA, Farraj SA, Hassan AM, Al-Saeed MS. 4.  et al. 2014. Evidence for camel-to-human transmission of MERS coronavirus. N. Engl. J. Med. 370:2499–505 [Google Scholar]
  5. Babkin IV, Tyumentsev AI, Tikunov AY, Kurilshikov AM, Ryabchikova EI. 5.  et al. 2013. Evolutionary time-scale of primate bocaviruses. Infect. Genet. Evol. 14:265–74 [Google Scholar]
  6. Bedford T, Riley S, Barr IG, Broor S, Chadha M. 6.  et al. 2015. Global circulation patterns of seasonal influenza viruses vary with antigenic drift. Nature 523:217–20 [Google Scholar]
  7. Biek R, Henderson JC, Waller LA, Rupprecht CE, Real LA. 7.  2007. A high-resolution genetic signature of demographic and spatial expansion in epizootic rabies virus. PNAS 104:7993–98 [Google Scholar]
  8. Bloomquist EW, Lemey P, Suchard MA. 8.  2010. Three roads diverged? Routes to phylogeographic inference. Trends Ecol. Evol. 25:626–32 [Google Scholar]
  9. Boni MF, Zhou Y, Taubenberger JK, Holmes EC. 9.  2008. Homologous recombination is very rare or absent in human influenza A virus. J. Virol. 82:4807–11 [Google Scholar]
  10. Bozick BA, Real LA. 10.  2015. The role of human transportation networks in mediating the genetic structure of seasonal influenza in the United States. PLOS Pathog. 11:e1004898 [Google Scholar]
  11. Bright RA, Medina MJ, Xu X, Perez-Oronoz G, Wallis TR. 11.  et al. 2005. Incidence of adamantane resistance among influenza A (H3N2) viruses isolated worldwide from 1994 to 2005: a cause for concern. Lancet 366:1175–81 [Google Scholar]
  12. Bromham L, Penny D. 12.  2003. The modern molecular clock. Nat. Rev. Genet. 4:216–24 [Google Scholar]
  13. Buhnerkempe MG, Gostic K, Park M, Ahsan P, Belser JA, Lloyd-Smith JO. 13.  2015. Mapping influenza transmission in the ferret model to transmission in humans. eLife 4:e07969 [Google Scholar]
  14. Carroll SM, Higa HH, Paulson JC. 14.  1981. Different cell-surface receptor determinants of antigenically similar influenza-virus hemagglutinins. J. Biol. Chem. 256:8357–63 [Google Scholar]
  15. Cauchemez S, Bhattarai A, Marchbanks TL, Fagan RP, Ostroff S. 15.  et al. 2011. Role of social networks in shaping disease transmission during a community outbreak of 2009 H1N1 pandemic influenza. PNAS 108:2825–30 [Google Scholar]
  16. Chare ER, Gould EA, Holmes EC. 16.  2003. Phylogenetic analysis reveals a low rate of homologous recombination in negative-sense RNA viruses. J. Gen. Virol. 84:2691–703 [Google Scholar]
  17. Cheng X, Tan Y, He M, Lam TT-Y, Lu X. 17.  et al. 2013. Epidemiological dynamics and phylogeography of influenza virus in southern China. J. Infect. Dis. 207:106–14 [Google Scholar]
  18. Cottam EM, Thebaud G, Wadsworth J, Gloster J, Mansley L. 18.  et al. 2008. Integrating genetic and epidemiological data to determine transmission pathways of foot-and-mouth disease virus. Proc. Biol. Sci. 275:887–95 [Google Scholar]
  19. Cui J, Eden JS, Holmes EC, Wang LF. 19.  2013. Adaptive evolution of bat dipeptidyl peptidase 4 (dpp4): implications for the origin and emergence of Middle East respiratory syndrome coronavirus. Virol. J. 10:304 [Google Scholar]
  20. Darling AE, Jospin G, Lowe E, Matsen FA IV, Bik HM, Eisen JA. 20.  2014. PhyloSift: phylogenetic analysis of genomes and metagenomes. PeerJ 2:e243 [Google Scholar]
  21. Diaz NN, Krause L, Goesmann A, Niehaus K, Nattkemper TW. 21.  2009. TACOA: taxonomic classification of environmental genomic fragments using a kernelized nearest neighbor approach. BMC Bioinform. 10:56 [Google Scholar]
  22. Do LAH, Wilm A, van Doorn HR, Lam HM, Sim S. 22.  et al. 2015. Direct whole-genome deep-sequencing of human respiratory syncytial virus A and B from Vietnamese children identifies distinct patterns of inter- and intra-host evolution. J. Gen. Virol. 96:3470–83 [Google Scholar]
  23. Drake JW, Holland JJ. 23.  1999. Mutation rates among RNA viruses. PNAS 96:13910–13 [Google Scholar]
  24. Drummond AJ, Pybus OG, Rambaut A, Forsberg R, Rodrigo AG. 24.  2003. Measurably evolving populations. Trends Ecol. Evol. 18:481–88 [Google Scholar]
  25. Drummond AJ, Rambaut A. 25.  2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7:214 [Google Scholar]
  26. Ducatez MF, Bahl J, Griffin Y, Stigger-Rosser E, Franks J. 26.  et al. 2011. Feasibility of reconstructed ancestral H5N1 influenza viruses for cross-clade protective vaccine development. PNAS 108:349–54 [Google Scholar]
  27. Duffy S, Shackelton LA, Holmes EC. 27.  2008. Rates of evolutionary change in viruses: patterns and determinants. Nat. Rev. Genet. 9:267–76 [Google Scholar]
  28. Edge R, Heath J, Rowlingson B, Keegan TJ, Isba R. 28.  2015. Seasonal influenza vaccination amongst medical students: a social network analysis based on a cross-sectional study. PLOS ONE 10:e0140085 [Google Scholar]
  29. Everitt AR, Clare S, Pertel T, John SP, Wash RS. 29.  et al. 2012. IFITM3 restricts the morbidity and mortality associated with influenza. Nature 484:519–23 [Google Scholar]
  30. Ewing G, Nicholls G, Rodrigo A. 30.  2004. Using temporally spaced sequences to simultaneously estimate migration rates, mutation rate and population sizes in measurably evolving populations. Genetics 168:2407–20 [Google Scholar]
  31. Felsenstein J. 31.  1983. Phylogenies and the comparative method. Am. Nat. 125:1–15 [Google Scholar]
  32. Feng Y, He X, Hsi JH, Li F, Li X. 32.  et al. 2013. The rapidly expanding CRF01_AE epidemic in China is driven by multiple lineages of HIV-1 viruses introduced in the 1990s. AIDS 27:1793–802 [Google Scholar]
  33. Firth C, Lipkin WI. 33.  2013. The genomics of emerging pathogens. Annu. Rev. Genom. Hum. Genet. 14:281–300 [Google Scholar]
  34. Foll M, Poh YP, Renzette N, Ferrer-Admetlla A, Bank C. 34.  et al. 2014. Influenza virus drug resistance: a time-sampled population genetics perspective. PLOS Genet. 10:e1004185 [Google Scholar]
  35. Frost SD, Volz EM. 35.  2010. Viral phylodynamics and the search for an ‘effective number of infections.’. Philos. Trans. R. Soc. Lond. B 365:1879–90 [Google Scholar]
  36. Gao R, Cao B, Hu Y, Feng Z, Wang D. 36.  et al. 2013. Human infection with a novel avian-origin influenza A (H7N9) virus. N. Engl. J. Med. 368:1888–97 [Google Scholar]
  37. Garcia J, Sovero M, Torres AL, Gomez J, Douce R. 37.  et al. 2009. Antiviral resistance in influenza viruses circulating in Central and South America based on the detection of established genetic markers. Influenza Respir. Viruses 3:69–74 [Google Scholar]
  38. Gaunt ER, Jansen RR, Poovorawan Y, Templeton KE, Toms GL, Simmonds P. 38.  2011. Molecular epidemiology and evolution of human respiratory syncytial virus and human metapneumovirus. PLOS ONE 6:e17427 [Google Scholar]
  39. Ghedin E, Holmes EC, DePasse JV, Pinilla LT, Fitch A. 39.  et al. 2012. Presence of oseltamivir-resistant pandemic A/H1N1 minor variants before drug therapy with subsequent selection and transmission. J. Infect. Dis. 206:1504–11 [Google Scholar]
  40. Ghedin E, Laplante J, DePasse J, Wentworth DE, Santos RP. 40.  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. 203:168–74 [Google Scholar]
  41. Grafen A. 41.  1989. The phylogenetic regression. Philos. Trans. R. Soc. Lond. B 326:119–57 [Google Scholar]
  42. Graham RL, Baric RS. 42.  2010. Recombination, reservoirs, and the modular spike: mechanisms of coronavirus cross-species transmission. J. Virol. 84:3134–46 [Google Scholar]
  43. Grenfell BT, Pybus OG, Gog JR, Wood JL, Daly JM. 43.  et al. 2004. Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303:327–32 [Google Scholar]
  44. Guan Y, Zheng BJ, He YQ, Liu XL, Zhuang ZX. 44.  et al. 2003. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302:276–78 [Google Scholar]
  45. Hall CB, Walsh EE, Long CE, Schnabel KC. 45.  1991. Immunity to and frequency of reinfection with respiratory syncytial virus. J. Infect. Dis. 163:693–98 [Google Scholar]
  46. Hay AJ, Zambon MC, Wolstenholme AJ, Skehel JJ, Smith MH. 46.  1986. Molecular basis of resistance of influenza A viruses to amantadine. J. Antimicrob. Chemother. 18:Suppl. B19–29 [Google Scholar]
  47. Heled J, Drummond AJ. 47.  2008. Bayesian inference of population size history from multiple loci. BMC Evol. Biol. 8:289 [Google Scholar]
  48. Hensley SE, Das SR, Bailey AL, Schmidt LM, Hickman HD. 48.  et al. 2009. Hemagglutinin receptor binding avidity drives influenza A virus antigenic drift. Science 326:734–36 [Google Scholar]
  49. Hensley SE, Das SR, Gibbs JS, Bailey AL, Schmidt LM. 49.  et al. 2011. Influenza A virus hemagglutinin antibody escape promotes neuraminidase antigenic variation and drug resistance. PLOS ONE 6:e15190 [Google Scholar]
  50. Hoffmann B, Tappe D, Hoper D, Herden C, Boldt A. 50.  et al. 2015. A variegated squirrel bornavirus associated with fatal human encephalitis. N. Engl. J. Med. 373:154–62 [Google Scholar]
  51. Holmes EC. 51.  2008. Evolutionary history and phylogeography of human viruses. Annu. Rev. Microbiol. 62:307–28 [Google Scholar]
  52. Holmes EC. 52.  2009. The Evolution and Emergence of RNA Viruses Oxford, UK: Oxford Univ. Press
  53. Holmes EC, Ghedin E, Halpin RA, Stockwell TB, Zhang XQ. 53.  et al. 2011. Extensive geographical mixing of 2009 human H1N1 influenza A virus in a single university community. J. Virol. 85:6923–29 [Google Scholar]
  54. Hon C-C, Lam TT-Y, Drummond A, Rambaut A, Lee Y-F. 54.  et al. 2006. Phylogenetic analysis reveals a correlation between the expansion of very virulent infectious bursal disease virus and reassortment of its genome segment B. J. Virol. 80:8503–9 [Google Scholar]
  55. Hon C-C, Lam TT-Y, Shi Z-L, Drummond AJ, Yip C-W. 55.  et al. 2008. Evidence of the recombinant origin of a bat severe acute respiratory syndrome (SARS)-like coronavirus and its implications on the direct ancestor of SARS coronavirus. J. Virol. 82:1819–26 [Google Scholar]
  56. Horimoto T, Kawaoka Y. 56.  2005. Influenza: lessons from past pandemics, warnings from current incidents. Nat. Rev. Microbiol. 3:591–600 [Google Scholar]
  57. Hue S, Pillay D, Clewley JP, Pybus OG. 57.  2005. Genetic analysis reveals the complex structure of HIV-1 transmission within defined risk groups. PNAS 102:4425–29 [Google Scholar]
  58. Ince WL, Gueye-Mbaye A, Bennink JR, Yewdell JW. 58.  2013. Reassortment complements spontaneous mutation in influenza A virus NP and M1 genes to accelerate adaptation to a new host. J. Virol. 87:4330–38 [Google Scholar]
  59. Jetzt AE, Yu H, Klarmann GJ, Ron Y, Preston BD, Dougherty JP. 59.  2000. High rate of recombination throughout the human immunodeficiency virus type 1 genome. J. Virol. 74:1234–40 [Google Scholar]
  60. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D. 60.  et al. 2008. Global trends in emerging infectious diseases. Nature 451:990–93 [Google Scholar]
  61. Kapoor A, Simmonds P, Slikas E, Li L, Bodhidatta L. 61.  et al. 2010. Human bocaviruses are highly diverse, dispersed, recombination prone, and prevalent in enteric infections. J. Infect. Dis. 201:1633–43 [Google Scholar]
  62. Kapusinszky B, Mulvaney U, Jasinska AJ, Deng X, Freimer N, Delwart E. 62.  2015. Local virus extinctions following a host population bottleneck. J. Virol. 89:8152–61 [Google Scholar]
  63. Kobayashi Y, Suzuki Y. 63.  2012. Evidence for N-glycan shielding of antigenic sites during evolution of human influenza A virus hemagglutinin. J. Virol. 86:3446–51 [Google Scholar]
  64. Kosakovsky Pond SL, Frost SD. 64.  2005. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol. Biol. Evol. 22:1208–22 [Google Scholar]
  65. Kosakovsky Pond SL, Poon AF, Leigh Brown AJ, Frost SD. 65.  2008. A maximum likelihood method for detecting directional evolution in protein sequences and its application to influenza A virus. Mol. Biol. Evol. 25:1809–24 [Google Scholar]
  66. Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SD. 66.  2006. Automated phylogenetic detection of recombination using a genetic algorithm. Mol. Biol. Evol. 23:1891–901 [Google Scholar]
  67. Kryazhimskiy S, Dushoff J, Bazykin GA, Plotkin JB. 67.  2011. Prevalence of epistasis in the evolution of influenza A surface proteins. PLOS Genet. 7:e1001301 [Google Scholar]
  68. Lai MM, Cavanagh D. 68.  1997. The molecular biology of coronaviruses. Adv. Virus Res. 48:1–100 [Google Scholar]
  69. Lam TT-Y, Chong YL, Shi M, Hon C-C, Li J. 69.  et al. 2013. Systematic phylogenetic analysis of influenza A virus reveals many novel mosaic genome segments. Infect. Genet. Evol. 18:367–78 [Google Scholar]
  70. Lam TT-Y, Hon C-C, Lemey P, Pybus OG, Shi M. 70.  et al. 2012. Phylodynamics of H5N1 avian influenza virus in Indonesia. Mol. Ecol. 21:3062–77 [Google Scholar]
  71. Lam TT-Y, Hon C-C, Pybus OG, Kosakovsky Pond SL, Wong RT. 71.  et al. 2008. Evolutionary and transmission dynamics of reassortant H5N1 influenza virus in Indonesia. PLOS Pathog. 4:e1000130 [Google Scholar]
  72. Lam TT-Y, Hon C-C, Tang JW. 72.  2010. Use of phylogenetics in the molecular epidemiology and evolutionary studies of viral infections. Crit. Rev. Clin. Lab. Sci. 47:5–49 [Google Scholar]
  73. Lam TT-Y, Hon C-C, Wang Z, Hui RK-H, Zeng F, Leung FC-C. 73.  2008. Evolutionary analyses of European H1N2 swine influenza A virus by placing timestamps on the multiple reassortment events. Virus Res. 131:271–78 [Google Scholar]
  74. Lam TT-Y, Ip HS, Ghedin E, Wentworth DE, Halpin RA. 74.  et al. 2012. Migratory flyway and geographical distance are barriers to the gene flow of influenza virus among North American birds. Ecol. Lett. 15:24–33 [Google Scholar]
  75. Lam TT-Y, Liu W, Bowden TA, Cui N, Zhuang L. 75.  et al. 2013. Evolutionary and molecular analysis of the emergent severe fever with thrombocytopenia syndrome virus. Epidemics 5:1–10 [Google Scholar]
  76. Lam TT-Y, Wang J, Shen Y, Zhou B, Duan L. 76.  et al. 2013. The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature 502:241–44 [Google Scholar]
  77. Lam TT-Y, Zhou B, Wang J, Chai Y, Shen Y. 77.  et al. 2015. Dissemination, divergence and establishment of H7N9 influenza viruses in China. Nature 522:102–5 [Google Scholar]
  78. Lamson D, Renwick N, Kapoor V, Liu Z, Palacios G. 78.  et al. 2006. MassTag polymerase-chain-reaction detection of respiratory pathogens, including a new rhinovirus genotype, that caused influenza-like illness in New York State during 2004–2005. J. Infect. Dis. 194:1398–402 [Google Scholar]
  79. Lax S, Smith DP, Hampton-Marcell J, Owens SM, Handley KM. 79.  et al. 2014. Longitudinal analysis of microbial interaction between humans and the indoor environment. Science 345:1048–52 [Google Scholar]
  80. Lee RT, Santos CL, de Paiva TM, Cui L, Sirota FL. 80.  et al. 2010. All that glitters is not gold—founder effects complicate associations of flu mutations to disease severity. Virol. J. 7:297 [Google Scholar]
  81. Lemey P, Pybus OG, Rambaut A, Drummond AJ, Robertson DL. 81.  et al. 2004. The molecular population genetics of HIV-1 group O. Genetics 167:1059–68 [Google Scholar]
  82. Lemey P, Rambaut A, Drummond AJ, Suchard MA. 82.  2009. Bayesian phylogeography finds its roots. PLOS Comput. Biol. 5:e1000520 [Google Scholar]
  83. Lemey P, Rambaut A, Welch JJ, Suchard MA. 83.  2010. Phylogeography takes a relaxed random walk in continuous space and time. Mol. Biol. Evol. 27:1877–85 [Google Scholar]
  84. Leventhal GE, Gunthard HF, Bonhoeffer S, Stadler T. 84.  2014. Using an epidemiological model for phylogenetic inference reveals density dependence in HIV transmission. Mol. Biol. Evol. 31:6–17 [Google Scholar]
  85. Li CX, Shi M, Tian JH, Lin XD, Kang YJ. 85.  et al. 2015. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. eLife 4:e05378 [Google Scholar]
  86. Li F, Li W, Farzan M, Harrison SC. 86.  2005. Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science 309:1864–68 [Google Scholar]
  87. Li H, Durbin R. 87.  2011. Inference of human population history from individual whole-genome sequences. Nature 475:493–96 [Google Scholar]
  88. Li LL, Delwart E. 88.  2011. From orphan virus to pathogen: the path to the clinical lab. Curr. Opin. Virol. 1:282–88 [Google Scholar]
  89. Li Q, Zhou L, Zhou M, Chen Z, Li F. 89.  et al. 2014. Epidemiology of human infections with avian influenza A(H7N9) virus in China. N. Engl. J. Med. 370:520–32 [Google Scholar]
  90. Li W, Shi Z, Yu M, Ren W, Smith C. 90.  et al. 2005. Bats are natural reservoirs of SARS-like coronaviruses. Science 310:676–79 [Google Scholar]
  91. Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS. 91.  et al. 1999. Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J. Virol. 73:152–60 [Google Scholar]
  92. Luksza M, Lassig M. 92.  2014. A predictive fitness model for influenza. Nature 507:57–61 [Google Scholar]
  93. Marklewitz M, Zirkel F, Kurth A, Drosten C, Junglen S. 93.  2015. Evolutionary and phenotypic analysis of live virus isolates suggests arthropod origin of a pathogenic RNA virus family. PNAS 112:7536–41 [Google Scholar]
  94. Martin DP, Posada D, Crandall KA, Williamson C. 94.  2005. A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res. Hum. Retroviruses 21:98–102 [Google Scholar]
  95. Martinelli M, Frati ER, Zappa A, Ebranati E, Bianchi S. 95.  et al. 2014. Phylogeny and population dynamics of respiratory syncytial virus (Rsv) A and B. Virus Res. 189:293–302 [Google Scholar]
  96. McIntyre CL, Savolainen-Kopra C, Hovi T, Simmonds P. 96.  2013. Recombination in the evolution of human rhinovirus genomes. Arch. Virol. 158:1497–515 [Google Scholar]
  97. McKimm-Breschkin JL. 97.  2000. Resistance of influenza viruses to neuraminidase inhibitors—a review. Antiviral Res. 47:1–17 [Google Scholar]
  98. Memish ZA, Mishra N, Olival KJ, Fagbo SF, Kapoor V. 98.  et al. 2013. Middle East respiratory syndrome coronavirus in bats, Saudi Arabia. Emerg. Infect. Dis. 19:1819–23 [Google Scholar]
  99. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL. 99.  2012. Detecting individual sites subject to episodic diversifying selection. PLOS Genet. 8:e1002764 [Google Scholar]
  100. Nelson MI, Stratton J, Killian ML, Janas-Martindale A, Vincent AL. 100.  2015. Continual reintroduction of human pandemic H1N1 influenza A viruses into swine in the United States, 2009 to 2014. J. Virol. 89:6218–26 [Google Scholar]
  101. Parrish CR, Holmes EC, Morens DM, Park EC, Burke DS. 101.  et al. 2008. Cross-species virus transmission and the emergence of new epidemic diseases. Microbiol. Mol. Biol. Rev. 72:457–70 [Google Scholar]
  102. Parrish CR, Murcia PR, Holmes EC. 102.  2015. Influenza virus reservoirs and intermediate hosts: dogs, horses, and new possibilities for influenza virus exposure of humans. J. Virol. 89:2990–94 [Google Scholar]
  103. Patterson Ross Z, Komadina N, Deng YM, Spirason N, Kelly HA. 103.  et al. 2015. Inter-seasonal influenza is characterized by extended virus transmission and persistence. PLOS Pathog. 11:e1004991 [Google Scholar]
  104. Pomeroy LW, Bjornstad ON, Holmes EC. 104.  2008. The evolutionary and epidemiological dynamics of the Paramyxoviridae. J. Mol. Evol. 66:98–106 [Google Scholar]
  105. Poon LL, Song T, Rosenfeld R, Lin X, Rogers MB. 105.  et al. 2016. Quantifying influenza virus diversity and transmission in humans. Nat. Genet. 48:195–200 [Google Scholar]
  106. Pupko T, Pe'er I, Shamir R, Graur D. 106.  2000. A fast algorithm for joint reconstruction of ancestral amino acid sequences. Mol. Biol. Evol. 17:890–96 [Google Scholar]
  107. Pybus OG, Charleston MA, Gupta S, Rambaut A, Holmes EC, Harvey PH. 107.  2001. The epidemic behavior of the hepatitis C virus. Science 292:2323–25 [Google Scholar]
  108. Pybus OG, Rambaut A, Harvey PH. 108.  2000. An integrated framework for the inference of viral population history from reconstructed genealogies. Genetics 155:1429–37 [Google Scholar]
  109. Raj VS, Mou HH, Smits SL, Dekkers DHW, Muller MA. 109.  et al. 2013. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495:251–54 [Google Scholar]
  110. Rambaut A, Holmes E. 110.  2009. The early molecular epidemiology of the swine-origin A/H1N1 human influenza pandemic. PLOS Curr. 1:RRN1003 [Google Scholar]
  111. Rambaut A, Pybus OG, Nelson MI, Viboud C, Taubenberger JK, Holmes EC. 111.  2008. The genomic and epidemiological dynamics of human influenza A virus. Nature 453:615–19 [Google Scholar]
  112. Reanney DC. 112.  1982. The evolution of RNA viruses. Annu. Rev. Microbiol. 36:47–73 [Google Scholar]
  113. Ren W, Qu XX, Li WD, Han ZG, Yu M. 113.  et al. 2008. Difference in receptor usage between severe acute respiratory syndrome (SARS) coronavirus and SARS-like coronavirus of bat origin. J. Virol. 82:1899–907 [Google Scholar]
  114. Roux S, Faubladier M, Mahul A, Paulhe N, Bernard A. 114.  et al. 2011. Metavir: a web server dedicated to virome analysis. Bioinformatics 27:3074–75 [Google Scholar]
  115. Russell CA, Jones TC, Barr IG, Cox NJ, Garten RJ. 115.  et al. 2008. The global circulation of seasonal influenza A (H3N2) viruses. Science 320:340–46 [Google Scholar]
  116. Sabir JS, Lam TT-Y, Ahmed MM, Li L, Shen Y. 116.  et al. 2015. Co-circulation of three camel coronavirus species and recombination of MERS-CoVs in Saudi Arabia. Science 351:81–84 [Google Scholar]
  117. Schmieder R, Edwards R. 117.  2011. Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–64 [Google Scholar]
  118. Scholtissek C. 118.  1990. Pigs as the ‘mixing vessel’ for the creation of new pandemic influenza A viruses. Med. Princip. Prac. 2:65–71 [Google Scholar]
  119. Sharp CP, LeBreton M, Kantola K, Nana A, Diffo Jle D. 119.  et al. 2010. Widespread infection with homologues of human parvoviruses B19, PARV4, and human bocavirus of chimpanzees and gorillas in the wild. J. Virol. 84:10289–96 [Google Scholar]
  120. Shi M, Lin XD, Vasilakis N, Tian JH, Li CX. 120.  et al. 2016. Divergent viruses discovered in arthropods and vertebrates revise the evolutionary history of the Flaviviridae and related viruses. J. Virol. 90:659–69 [Google Scholar]
  121. Shimodaira H, Hasegawa M. 121.  1999. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16:1114–16 [Google Scholar]
  122. Shinya K, Ebina M, Yamada S, Ono M, Kasai N, Kawaoka Y. 122.  2006. Influenza virus receptors in the human airway. Nature 440:435–36 [Google Scholar]
  123. Simmonds P, Welch J. 123.  2006. Frequency and dynamics of recombination within different species of human enteroviruses. J. Virol. 80:483–93 [Google Scholar]
  124. Simon-Loriere E, Holmes EC. 124.  2011. Why do RNA viruses recombine?. Nat. Rev. Microbiol. 9:617–26 [Google Scholar]
  125. Simonsen L, Viboud C, Grenfell BT, Dushoff J, Jennings L. 125.  et al. 2007. The genesis and spread of reassortment human influenza A/H3N2 viruses conferring adamantane resistance. Mol. Biol. Evol. 24:1811–20 [Google Scholar]
  126. Slatkin M, Hudson RR. 126.  1991. Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–62 [Google Scholar]
  127. Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF. 127.  et al. 2004. Mapping the antigenic and genetic evolution of influenza virus. Science 305:371–76 [Google Scholar]
  128. Song HD, Tu CC, Zhang GW, Wang SY, Zheng K. 128.  et al. 2005. Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. PNAS 102:2430–35 [Google Scholar]
  129. Stack JC, Murcia PR, Grenfell BT, Wood JL, Holmes EC. 129.  2013. Inferring the inter-host transmission of influenza A virus using patterns of intra-host genetic variation. Proc. Biol. Sci. 280:20122173 [Google Scholar]
  130. Stadler T, Kouyos R, von Wyl V, Yerly S, Boni J. 130.  et al. 2012. Estimating the basic reproductive number from viral sequence data. Mol. Biol. Evol. 29:347–57 [Google Scholar]
  131. Stadler T, Kuhnert D, Bonhoeffer S, Drummond AJ. 131.  2013. Birth-death skyline plot reveals temporal changes of epidemic spread in HIV and hepatitis C virus (HCV). PNAS 110:228–33 [Google Scholar]
  132. Stavrinides J, Guttman DS. 132.  2004. Mosaic evolution of the severe acute respiratory syndrome coronavirus. J. Virol. 78:76–82 [Google Scholar]
  133. Su YC, Bahl J, Joseph U, Butt KM, Peck HA. 133.  et al. 2015. Phylodynamics of H1N1/2009 influenza reveals the transition from host adaptation to immune-driven selection. Nat. Commun. 6:7952 [Google Scholar]
  134. Sullender WM. 134.  2000. Respiratory syncytial virus genetic and antigenic diversity. Clin. Microbiol. Rev. 13:1–15 [Google Scholar]
  135. Sweet C, Hayden FG, Jakeman KJ, Grambas S, Hay AJ. 135.  1991. Virulence of rimantadine-resistant human influenza A (H3N2) viruses in ferrets. J. Infect. Dis. 164:969–72 [Google Scholar]
  136. Taft AS, Ozawa M, Fitch A, Depasse JV, Halfmann PJ. 136.  et al. 2015. Identification of mammalian-adapting mutations in the polymerase complex of an avian H5N1 influenza virus. Nat. Commun. 6:7491 [Google Scholar]
  137. Tong S, Zhu X, Li Y, Shi M, Zhang J. 137.  et al. 2013. New world bats harbor diverse influenza A viruses. PLOS Pathog. 9:e1003657 [Google Scholar]
  138. van Riel D, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RAM. 138.  et al. 2006. H5N1 virus attachment to lower respiratory tract. Science 312:399 [Google Scholar]
  139. Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R. 139.  2006. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439:344–48 [Google Scholar]
  140. Vijaykrishna D, Holmes EC, Joseph U, Fourment M, Su YC. 140.  et al. 2015. The contrasting phylodynamics of human influenza B viruses. eLife 4:e05055 [Google Scholar]
  141. Volz EM, Frost SD. 141.  2014. Sampling through time and phylodynamic inference with coalescent and birth-death models. J. R. Soc. Interface 11:20140945 [Google Scholar]
  142. Waller LA, Gotway CA. 142.  2004. Spatial Epidemiology: Methods and Applications Oxford, UK: Oxford Univ. Press
  143. Wang W, Lin XD, Guo WP, Zhou RH, Wang MR. 143.  et al. 2015. Discovery, diversity and evolution of novel coronaviruses sampled from rodents in China. Virology 474:19–27 [Google Scholar]
  144. Wilker PR, Dinis JM, Starrett G, Imai M, Hatta M. 144.  et al. 2013. Selection on haemagglutinin imposes a bottleneck during mammalian transmission of reassortant H5N1 influenza viruses. Nat. Commun. 4:2636 [Google Scholar]
  145. Wommack KE, Bhavsar J, Polson SW, Chen J, Dumas M. 145.  et al. 2012. VIROME: a standard operating procedure for analysis of viral metagenome sequences. Stand. Genom. Sci. 6:427–39 [Google Scholar]
  146. Yamada S, Suzuki Y, Suzuki T, Le MQ, Nidom CA. 146.  et al. 2006. Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature 444:378–82 [Google Scholar]
  147. Yang Z, Wong WS, Nielsen R. 147.  2005. Bayes empirical Bayes inference of amino acid sites under positive selection. Mol. Biol. Evol. 22:1107–18 [Google Scholar]
  148. Yen HL, Herlocher LM, Hoffmann E, Matrosovich MN, Monto AS. 148.  et al. 2005. Neuraminidase inhibitor-resistant influenza viruses may differ substantially in fitness and transmissibility. Antimicrob. Agents Chemother. 49:4075–84 [Google Scholar]
  149. Ypma RJ, Bataille AM, Stegeman A, Koch G, Wallinga J, van Ballegooijen WM. 149.  2012. Unravelling transmission trees of infectious diseases by combining genetic and epidemiological data. Proc. Biol. Sci. 279:444–50 [Google Scholar]
  150. Yu H, Cowling BJ, Feng L, Lau EH, Liao Q. 150.  et al. 2013. Human infection with avian influenza A H7N9 virus: an assessment of clinical severity. Lancet 382:138–45 [Google Scholar]

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