The evolutionary genetics of emerging viruses

Annual Review of Ecology, Evolution, and Systematics

Volumn 40, Issue , 2009, Pages 353-372

  Holmes, Edward C ^a,b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Complementation; Emergence; Epistasis; Evolution; Fitness; Mutation; Natural selection; Quasispecies; Recombination; RNA secondary structure; Robustness

Indexed keywords

ADAPTATION; EMERGENCE; EPISTASIS; EVOLUTION; FITNESS; GENETIC VARIATION; GENOME; HOST USE; MUTATION; NATURAL SELECTION; POPULATION GENETICS; POPULATION SIZE; RECOMBINATION; RNA; VIRUS;

RNA VIRUSES;

EID: 77951692453     PISSN: 1543592X     EISSN: 15452069     Source Type: Book Series    
DOI: 10.1146/annurev.ecolsys.110308.120248     Document Type: Article

References (120)

1. Aaskov J, Buzacott K, Thu HM, Lowry K, Holmes EC. 2006. Long-term transmission of defective RNA viruses in humans and Aedes mosquitoes. Science 311:236-238
2. Anderson JP, Daifuku R, Loeb LA. 2004. Viral error catastrophe by mutagenic nucleosides. Annu. Rev. Mi-crobiol. 58:183-205
3. Antia R, Regoes RR, Koella JC, Bergstrom CT. 2003. The role of evolution in the emergence of infectious diseases. Nature 426:658-661
4. Arai S, Bennett SN, Sumibcay L, Cook JA, Song JW, et al. 2008. Phylogenetically distinct hantaviruses in the masked shrew (Sorex cinereus) and dusky shrew (Sorex monticolus) in the United States. Am. J. Trop. Med. Hyg. 78:348-351
5. Archer AM, Rico-Hesse R. 2002. High genetic divergence and recombination in arenaviruses from the Americas. Virology 304:274-281
6. Belshaw R, Pybus OG, Rambaut A. 2007. The evolution of genome compression in RNA viruses. Genome Res. 17:1496-1504
7. Bonhoeffer S, Chappey C, Parkin NT, Whitcomb JM, Petropoulos CJ. 2004. Evidence for positive epistasis in HIV-1. Science 306:1547-1550
8. Bull JJ, Meyers LA, Lachmann M. 2005. Quasispecies made simple. PLoS Comput. Biol. 1:e61
9. Bull JJ, Sanjuan R, Wilke CO. 2007. Theory of lethal mutagenesis for viruses. J. Virol. 81:2930-2939
10. Burch CL, Chao L. 2000. Evolvability of an RNA virus is determined by its mutational neighbourhood. Nature 406:625-628
11. Burch CL, Chao L. 2004. Epistasis and its relationshiptocanalization inthe RNA virus φ6. Genetics 167:559-567
12. Burch CL, Turner PE, Hanley KA. 2003. Patterns of epistasis in RNA viruses: a review of the evidence from vaccine design. J. Evol. Biol. 16:1223-1235
13. Burke DS. 1998. Evolvability of emerging viruses. In Pathology of Emerging Infections 2, ed. AM Nelson, CR Horsburgh Jr, pp. 1-12. Washington DC: Am. Soc. Microbiol.
14. Bush RM, Fitch WM, Bender CA, Cox NJ. 1999. Positive selection on the H3 hemagglutinin gene of human influenza virus A. Mol. Biol. Evol. 16:1457-1465
15. Carrillo C, Lu Z, Borca MV, Vagnozzi A, Kutish GF, Rock DL. 2007. Genetic and phenotypic variation of foot-and-mouth disease virus during serial passages in a natural host. J. Virol. 81:11341-11351
16. Chare ER, Gould EA, Holmes EC. 2003. Phylogenetic analysis revealsalow rateofhomologous recombination in negative-sense RNA viruses. J. Gen. Virol. 84:2691-2703
17. Chao D-Y, King C-C, Wang W-K, Chen W-J, Wu H-L, Chang G-J. 2005. Strategically examining the full-genome of dengue virus type 3 in clinical isolates reveals its mutation spectra. Virol. J. 2:72
18. Charrel RN, Feldmann H, Fulhorst CF, Khelifa R, de Chesse R, de Lamballerie X. 2002. Phylogeny of New World arenaviruses based on the complete coding sequences of the small genomic segment identified an evolutionary lineage produced by intrasegmental recombination. Biochem. Biophys. Res. Commun. 296:1118-1124
19. Cleaveland S, Laurenson MK, Taylor LH. 2001. Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Philos. Trans. R. Soc. London Ser. B 356:991-999
20. Codoñer FM, Daros JA, Sole RV, Elena SF. 2006. The fittest versus the flattest: experimental confirmation of the quasispecies effect with subviral pathogens. PLoS Pathog. 2:e136
21. Coffey LL, Vasilakis N, Brault AC, Powers AM, Tripet F, Weaver SC. 2008. Arbovirus evolution in vivo is constrained by host alternation. Proc. Natl. Acad. Sci. USA 105:6970-6975
22. Cole CN, Baltimore D. 1973. Defective interfering particles of poliovirus. III. Inference and enrichment. J. Mol. Biol. 76:345-361
23. Coleman JR, Papamichail D, Skiena S, Futcher B, Wimmer E, Mueller S. 2008. Virus attenuation by genome-scale changes in codon pair bias. Science 320:1784-1787
24. Comas I, Moya A, Gonzalez-Candelas F. 2005. Validating viral quasispecies with digital organisms: a re-examination of the critical mutation rate. BMC Evol. Biol. 5:5
25. Crotty S, Cameron CE, Andino R. 2001. RNA virus error catastrophe: direct test by using ribavirin. Proc. Natl. Acad. Sci. USA 98:6895-6900
26. de la Iglesia F, Elena SF. 2007. Fitness declines in tobacco etch virus upon serial bottleneck transfers. J. Virol. 81:4941-4947
27. de Visser JA, Hermisson J, Wagner GP, Ancel Meyers L, Bagheri-Chaichian H, et al. 2003. Evolution and detection of genetic robustness. Evolution 57:1959-1972
28. Domingo E. 2002. Quasispecies theory in virology. J. Virol. 76:463-465
29. Domingo E, Escarḿis C, Meńindez-Arias L, Holland JJ. 1999. Viral quasispecies and fitness variations. In Origin and Evolution of Viruses, ed. E Domingo, R Webster, JJ Holland, pp. 141-161 London: Academic
30. Domingo E, Holland JJ. 1997. RNA virus mutations for fitness and survival. Annu. Rev. Microbiol. 51:151-178
31. Domingo E, Sabo D, Taniguchi T, Weissman C. 1978. Nucleotide sequence heterogeneity of an RNA phage population. Cell 13:735-744
32. Drake JW. 1993. Rates of spontaneous mutation among RNA viruses. Proc. Natl. Acad. Sci. USA 90:4171-4175
33. Drake JW, Holland JJ. 1999. Mutation rates among RNA viruses. Proc. Natl. Acad. Sci. USA 96:13910-13913
34. Drummond AJ, Pybus OG, Rambaut A, Forsberg R, Rodrigo AG. 2003. Measurably evolving populations. Trends Ecol. Evol. 18:481-488
35. Duffy S, Shackelton LA, Holmes EC. 2008. Ratesofevolutionary changeinviruses: Patterns and determinants. Nat. Rev. Genet. 9:267-276
36. Edwards CTT, Holmes EC, Pybus OG, Wilson DJ, Viscidi RP, et al. 2006. Evolution of the HIV-1 envelope is dominated by purifying selection. Genetics 174:1441-1453
37. Eigen M. 1971. Self-organizationofmatter and the evolutionofbiological macromolecules. Naturwissenschaften 58:465-523
38. Eigen M. 1992. Steps Towards Life. New York: Oxford Univ. Press
39. Eigen M, Schuster P. 1977. The hypercycle, a principle of natural self-organization. Part A: Emergence of the hypercycle. Naturwissenschaften 64:541-565
40. Elena SF, Carrasco P, Daròs JA, Sanjuán R. 2006. Mechanisms of genetic robustness in RNA viruses. EMBO Rep. 7:168-173
41. Elena SF, Moya A. 1999. Rate of deleterious mutation and the distribution of its effects on fitness in vesicular stomatitis virus. J. Evol. Biol. 12:1078-1088
42. Elena SF, Sanjuán R. 2005. Adaptive value of high mutation rates of RNA viruses: separating causes from consequences. J. Virol. 79:11555-11558
43. Froissart R, Michalakis Y, Blanc S. 2002. Helper component- transcomplementation in the vector transmission of plant viruses. Phytopathology 92:576-579
44. Furió V, Moya A, Sanjaun R. 2005. The cost of replication fidelity in an RNA virus. Proc. Natl. Acad. Sci. USA 102:10233-10237
45. Furió V, Moya A, Sanjuán R. 2007. The cost of replication fidelity in human immunodeficiency virus type 1. Proc. Biol. Sci. 274:225-230
46. Garćia-Arriaza J, Manrubia SC, Toja M, Domingo E, Escarḿis C. 2004. Evolutionary transition toward defective RNAs that are infectious by complementation. J. Virol. 78:11678-11685
47. Gao F, Chen Y, Levy DN, Conway JA, Kepler TB, Hui H. 2004. Unselected mutations in the human immunodeficiency virus type 1 genome are most nonsynonymous and often deleterious. J. Virol. 78:2426-2433
48. Ghedin E, Fitch A, Boyne A, DePasse J, Bera J, et al. 2009. Mixed infection and the genesis of influenza diversity. J. Virol. In Press (doi:10. 1128/JVI. 00773-809)
49. Gibbs AJ, Gibbs MJ, Ohshima K, Garćia-Arenal F. 2008. More about plant virus evolution: past, present and future. In Origin and Evolution of Viruses, ed. E Domingo, CR Parrish, JJ Holland, pp. 229-250 London: Academic. 2nd ed.
50. Gorbalenya AE, Enjuanes L, Ziebuhr J, Snijder EJ. 2006. Nidovirales: evolving the largest RNA virus genome. Virus Res. 117:17-37
51. Greenbaum BD, Levine AJ, Bhanot G, Rabadan R. 2008. Patterns of evolution and host gene mimicry in influenza and other RNA viruses. PLoS Pathog. 4:e1000079
52. Hanada K, Suzuki Y, Gojobori T. 2004. A large variation in the rates of synonymous substitution for RNA viruses and its relationshiptoadiversityof viral infection and transmission modes. Mol. Biol. Evol. 21:1074-1080
53. Holmes EC. 2003a. Error thresholds and the constraints to RNA virus evolution. Trends Microbiol. 11:543-546
54. Holmes EC. 2003b. Patterns of intra-and interhost nonsynonymous variation reveal strong purifying selection in dengue virus. J. Virol. 77:11296-11298
55. Holmes EC. 2004. The phylogeography of human viruses. Mol. Ecol. 13:745-756
56. Holmes EC. 2006. The evolution of viral emergence. Proc. Natl. Acad. Sci. USA 103:4803-4804
57. Holmes EC. 2008. The evolutionary history and phylogeography of human viruses. Annu. Rev. Microbiol. 62:307-328
58. Holmes EC. 2009. The Evolution and Emergence of RNA Viruses, ed. PH Harvey, RM May. Oxford Ser. Ecol. Evol. (OSEE). Oxford: Oxford Univ. Press
59. Holmes EC, Moya A. 2002. Is the quasispecies concept relevant to RNA viruses? J. Virol. 76:460-462
60. Huang AS, Baltimore D. 1970. Defective viral particles and viral disease processes. Nature 226:325-327
61. Jenkins GM, Pagel M, Gould EA, Zanotto PM de A, Holmes EC. 2001. Evolution of base composition and codon usage bias in the genus Flavivirus. J. Mol. Evol. 52:383-390
62. Jenkins GM, Rambaut A, Pybus OG, Holmes EC. 2002. Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J. Mol. Evol. 54:152-161
63. Jerzak G, Bernard KA, Kramer LD, Ebel GD. 2005. Genetic variation in West Nile virus from naturally infected mosquitoes and birds suggests quasispecies structure and strong purifying selection. J. Gen. Virol. 86:2175-2183
64. Jetzt AE, YuH, Klarmann GJ, RonY, Preston BD, Dougherty JP. 2000. High rateofrecombination throughout the human immunodeficiency virus type 1 genome. J. Virol. 74:1234-1240
65. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, et al. 2008. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc. Natl. Acad. Sci. USA 105:7552-7557
66. Kondrashov AS. 1988. Deleterious mutations and the evolution of sexual reproduction. Nature 336:435-440
67. Krakauer DC, Plotkin JB. 2002. Redundancy, antiredundancy, and the robustness of genomes. Proc. Natl. Acad. Sci. USA 99:1405-1409
68. Kun A, Santos M, Szathmáry E. 2005. Real ribozymes suggest a relaxed error threshold. Nat. Genet. 37:1008-1011
69. Lai MMC. 1992. RNA recombination in animal and plant viruses. Microbiol. Rev. 56:61-79
70. Leigh Brown AJ. 1997. Analysis of HIV-1 env gene sequences reveals evidence for a low effective number in the viral population. Proc. Natl. Acad. Sci. USA 94:1862-1865
71. Malpica JM, Fraile A, Moreno I, Obies CI, Drake JW, et al. 2002. The rate and character of spontaneous mutation in an RNA virus. Genetics 162:1505-1511
72. Manrubia SC, Escarḿis C, Domingo E, Lázaro E. 2005. High mutation rates, bottlenecks, and robustness of RNA viral quasispecies. Gene 347:273-282
73. Mansky LM. 1998. Retrovirus mutation rates and their role in genetic variation. J. Gen. Virol. 79:1337-1345
74. Mansky LM, Cunningham KS. 2000. Virus mutators and antimutators: roles in evolution, pathogenesis and emergence. Trends Genet. 16:512-517
75. Mansky LM, Durand DP, Hill JH. 1995. Evidence for complementation of plant potyvirus pathogenic strains in mixed infection. J. Phytopathol. 143:247-250
76. Mansky LM, Temin HM. 1995. Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. J. Virol. 69:5087-5094
77. Marsh GA, Rabadán R, Levine AJ, Palese P. 2008. Highly conserved regions of influenza a virus polymerase gene segments are critical for efficient viral RNA packaging. J. Virol. 82:2295-2304
78. McMullanLK, GrakouiA, Evans MJ, Mihalik K, PuigM, etal. 2007. Evidence for a functional RNA element in the hepatitis C virus core gene. Proc. Natl. Acad. Sci. USA 104:2879-2884
79. Minskaia E, Hertzig T, Gorbalenya AE, Campanacci V, Cambillau C, et al. 2006. Discovery of an RNA virus 3' → 5' exoribonuclease that is critically involved in coronavirus RNA synthesis. Proc. Natl. Acad. Sci. USA 103:5108-5113
80. Miralles R, Gerrish PJ, Moya A, Elena SF. 1999. Clonal interference and the evolution of RNA viruses. Science 285:1745-1747
81. Montville R, Froissart R, Remold SK, Tenaillon O, Turner PE. 2005. Evolution of mutational robustness in an RNA virus. PLoSBiol. 3:e381
82. Moreno IM, Malpica JM, Rodŕiguez-Cerezo E, Garćia-Arenal F. 1997. A mutation in tomato aspermy cucu-movirus that abolishes cell-to-cell movement is maintained to high levels in the viral RNA population by complementation. J. Virol. 71:9157-9162
83. Morse SS. 1995. Factors in the emergence of infectious diseases. Emerg. Infect. Dis. 1:7-15
84. Moya A, Holmes EC, González-Candelas F. 2004. The population genetics and evolutionary epidemiology of RNA viruses. Nat. Rev. Microbiol. 2:279-287
85. Novella IS, Zárate S, Metzgar D, Ebendick-Corpus BE. 2004. Positive selection of synonymous mutations in vesicular stomatitis virus. J. Mol. Biol. 342:1415-1421
86. Palmemberg AC, SgroJ-Y. 1997. Topological organisation of picornaviral genomes: statistical prediction of RNA structural signals. Semin. Virol. 8:231-241
87. Pariente N, Sierra S, Lowenstein PR, Domingo E. 2001. Efficient virus extinction by combinations of a mutagen and antiviral inhibitors. J. Virol. 75:9723-9730
88. Parrish CR, Holmes EC, Morens DM, Park E-C, Burke DS, et al. 2008. Cross-species viral transmission and the emergence of new epidemic diseases. Microbiol. Mol. Biol. Rev. 72:457-470
89. Pelletier J, Sonenberg N. 1988. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 334:320-325
90. Perelson AS, Neumann AU, Markowitz M, Leonard JM, Ho DD. 1996. HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science 271:1582-1586
91. Pybus OG, Rambaut A, Freckleton RP, Belshaw R, Drummond AJ, Holmes EC. 2007. Phylogenetic evidence for deleterious mutation load in RNA viruses and its contribution to viral evolution. Mol. Biol. Evol. 24:845-852
92. Rabadán R, Levine AJ, Robins H. 2006. Comparison of avian and human influenza A viruses reveals a mutational bias on the viral genomes. J. Virol. 80:11887-11891
93. Ramsden C, Holmes EC, Charleston MA. 2008a. Hantavirus evolution in relation to its rodent and insectivore hosts: no evidence for codivergence. Mol. Biol. Evol. 26:143-153
94. Ramsden C, Melo FL, Figueiredo LM, Holmes EC, Zanotto PM de A, VGDN Consortium. 2008b. High rates of molecular evolution in hantaviruses. Mol. Biol. Evol. 25:1488-1492
95. Robertson MP, Igel H, Baertsch R, Haussler D, Ares M Jr, Scott WG 2005. The structure of a rigorously conserved RNA element within the SARS virus genome. PLoS Biol. 3:e5
96. Rouzine IM, Coffin JM. 1999. Linkage disequilibrium test implies a large effective population number for HIV in vivo. Proc. Natl. Acad. Sci. USA 96:10758-10763
97. Sanjuán R 2006. Quantifying antagonistic epistasis in a multifunctional RNA secondary structure of the Rous sarcoma virus. J. Gen. Virol. 87:1595-1602
98. Sanjuán R 2008. Quasispecies. In Encyclopedia of Virology, ed. BWJ Mahy, MHV Van Regenmortal, 4:359-365. Oxford, UK: Elsevier. 3rd ed.
99. Sanjuán R, Cuevas JM, Furió V, Holmes EC, Moya A. 2007. Selection for robustness in mutagenesized RNA viruses. PLoS Genet. 3:e93
100. Sanjuán R, Elena SF. 2006. Epistasis correlates to genomic complexity. Proc. Natl. Acad. Sci. USA 103:14402-14405
101. Sanjuán R, Forment J, Elena SF. 2006. In silico predicted robustness of viroid RNA secondary structures. II. Interaction between mutation pairs. Mol. Biol. Evol. 23:2123-2130
102. 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
103. 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 (Pubitemid 39441549)
104. Shapiro B, Rambaut A, Pybus OG, Drummond A, Holmes EC. 2006. A phylogenetic method for detecting positive epistasis in gene sequences and its application to RNA virus evolution. Mol. Biol. Evol. 23:1724-1730
105. Simmonds P, Smith DB. 1999. Structural constraints on RNA virus evolution. J. Virol. 73:5787-5794
106. Simmonds P, Tuplin A, Evans DJ. 2004. Detection of genome-scale ordered RNA structure (GORS) in genomes of positive-stranded RNA viruses: implications for virus evolution and host persistence. RNA 10:1337-1351
107. Simonsen L, Viboud C, Grenfell BT, Dushoff J, Jennings L, et al. 2007. The rapid global spread of reassortant human influenza A/H3N2 viruses conferring adamantane resistance. Mol. Biol. Evol. 24:1811-1820
108. Steinhauer DA, de la Torre JC, Meier E, Holland JJ. 1989. Extreme heterogeneity in populations of vesicular stomatitis virus. J. Virol. 63:2072-2080
109. Suzuki Y, Nei M. 2002. Simulation studyofthe reliability and robustness ofthe statistical methods for detecting positive selection at single amino acid sites. Mol. Biol. Evol. 11:1865-1869
110. Thurner C, Witwer C, Hofacker IL, Stadler PF. 2004. Conserved RNA secondary structures in Flaviviridae genomes. J. Gen. Virol. 85:1113-1124 (Pubitemid 38659775)
111. Teycheney PY, Laboureau N, Iskra-Caruana ML, Candresse T. 2005. High genetic variability and evidence for plant-to-plant transfer of banana mild mosaic virus. J. Gen. Virol. 86:3179-3187
112. Tzeng WP, Frey TK. 2003. Complementation of a deletion in the rubella virus p150 nonstructural protein by the viral capsid protein. J. Virol. 77:9502-9510
113. Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R. 2005. Quasispecies diversity determines patho-genesis through cooperative interactions in a viral population. Nature 439:344-348
114. Wilke CO. 2005. Quasispecies theory in the context of population genetics. BMC Evol. Biol. 5:44
115. Wilke CO, Lenski RE, Adami C. 2003. Compensatory mutations cause excess of antagonistic epistasis in RNA secondary structure folding. BMC Evol. Biol. 3:3
116. 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 412:331-333
117. Wittmann TJ, Biek R, Hassanin A, Rouquet P, Reed P, et al. 2007. Isolates of Zaire ebolavirus from wild apes reveal genetic lineage and recombinants. Proc. Natl. Acad. Sci. USA 104:17123-17127
118. Wolfe ND, Daszak P, Kilpatrick AM, Burke DS. 2005. Bushmeat hunting, deforestation, and prediction of zoonoses emergence. Emerg. Infect. Dis. 11:1822-1827
119. Woolhouse MEJ. 2002. Population biology of emerging and re-emerging pathogens. Trends Microbiol. 10:S3-7
120. Yang Z, Bielawski JP. 2000. Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15:496-502