The population genetics and evolutionary epidemiology of RNA viruses

Nature Reviews Microbiology

Volumn 2, Issue 4, 2004, Pages 279-288

  Moya, Andrés ^a   Holmes, Edward C ^b   González Candelas, Fernando ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; GENE TRANSLOCATION; GENETIC DRIFT; GENETIC EPIDEMIOLOGY; GENETIC VARIABILITY; GENOTYPE; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MEDICAL RESEARCH; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NATURAL SELECTION; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; REVIEW; RNA VIRUS; SARS CORONAVIRUS; SEQUENCE ANALYSIS; SEVERE ACUTE RESPIRATORY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VESICULAR STOMATITIS VIRUS; VIRAL GENETICS; VIRUS ATTENUATION; VIRUS MUTATION; VIRUS PARTICLE; VIRUS RECOMBINATION; VIRUS REPLICATION; VIRUS VIRULENCE; ANIMAL; BIOLOGICAL MODEL; EPIDEMIOLOGY; GENETIC SELECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MUTATION; PHYLOGENY; POPULATION GENETICS; RNA VIRUS INFECTION;

CORONAVIRUS; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; RNA VIRUSES; SARS CORONAVIRUS; SIMIAE; SIMIAN IMMUNODEFICIENCY VIRUS; VESICULAR STOMATITIS VIRUS;

ANIMALS; EPIDEMIOLOGY, MOLECULAR; EVOLUTION, MOLECULAR; GENETIC DRIFT; GENETICS, POPULATION; HUMANS; MODELS, GENETIC; MUTATION; PHYLOGENY; RNA VIRUS INFECTIONS; RNA VIRUSES; SELECTION (GENETICS);

EID: 2142753891     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro863     Document Type: Review

References (136)

1. Domingo, E. & Holland, J. J. RNA virus mutations and fitness for survival. Ann. Rev. Microbiol. 51, 151-178 (1997).
2. Domingo, E., Webster, R. & Holland J. (eds). Origin and Evolution of Viruses (Academic Press, London, 1999).
3. Grenfell, B. T. et al. Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303, 327-332 (2004).
4. Elena, S. F., Miralles, R. & Moya, A. Frequency-dependent selection in a mammalian RNA virus. Evolution 5, 984-987 (1997).
5. Drake, J. W. Rates of spontaneous mutation among RNA viruses. Proc. Natl Acad. Sci. USA 90, 4171-4175 (1993).
6. Malpica, J. M. et al. The rate and character of spontaneous mutation in an RNA virus. Genetics 162, 1505-1511 (2002).
7. Eigen, M. Self-organisation of matter and the evolution of biological macromolecules. Naturwissenschaften 58, 465 (1971).
8. Maynard Smith, J. & Szathmáry, E. The Major Transitions of Evolution. (W. H. Freeman & Co., Oxford, 1995).
9. Rouzine, I. M., Rodrigo, A. & Coffin, J. M. Transition between stochastic evolution and deterministic evolution in the presence of selection: general theory and application to virology. Microbiol. Mol. Biol. Rev. 65, 151-185 (2001).
10. Osada, D., Crandall, K. A. & Holmes, E. C. Recombination in evolutionary genomics. Ann. Rev. Genet. 36, 75-97 (2002).
11. Rhodes, T., Wargo, H. & Hu, W. S. High rates of human immunodeficiency virus type 1 recombination: near-random segregation of markers one kilobase apart in one round of viral replication. J. Virol. 77, 11193-11200 (2003).
12. Boerlijst, M. C., Bonhoeffer, S. & Nowak, M. A. Viral quasispecies and recombination. Proc. R. Soc. Lond. B Biol. Sci. 263, 1577-1584 (1996).
13. Chare, E. R., Gould, E. A. & Holmes, E. C. Phylogenetic analysis reveals a low rate of homologous recombination in negative-sense RNA viruses. J. Gen. Virol. 84, 2691-2703 (2003).
14. Navas, S., Martin, J., Quiroga, J. A., Castillo, I. & Carreño, V. Genetic diversity and tissue compartmentalization of the hepatitis C virus genome in blood mononuclear cells, liver, and serum from chronic hepatitis C patients. J. Virol. 72, 1640-1646 (1998).
15. Miralles, R., Moya, A. & Elena, S. F. Effect of population patchiness and migration rates on the adaptation and divergence of vesicular stomatitis virus quasispecies populations. J. Gen. Virol. 80, 2051-2059 (1999).
16. Eigen, M. & Schuster, P. The hypercycle. A principle of natural self-organization. Part A: emergence of the hypercycle. Naturwissenschaften 64, 541-565 (1977).
17. Eigen, M. Steps Towards Life (Oxford Univ. Press, New York, 1996).
18. Domingo, E., Sabo, D., Taniguchi, T. & Weissman, C. Nucleotide sequence heterogeneity of an RNA phage population. Cell 13, 735-744 (1978).
19. de la Torre, J. C. & Holland, J. J. RNA virus quasispecies populations can suppress vastly superior mutant progeny. J. Virol. 64, 6278-6281 (1990).
20. Jenkins, G. M., Worobey, M., Woelk, C. H. & Holmes, E. C. Evidence for the nonquasispecies evolution of RNA viruses. Mol. Biol. Evol. 18, 987-994 (2001).
21. Holmes, E. C. & Moya, A. Is the quasispecies concept relevant to RNA viruses? J. Virol. 76, 460-462 (2002).
22. Burch, C. L. & Chao, L. Evolvability of an RNA virus is determined by its mutational neighborhood. Nature 406, 625-628 (2000).
23. Wichman, H. A., Scott, L. A., Yarber, C. D. & Bull, J. J. Experimental evolution recapitulates natural evolution. Philos. Trans R. Soc. Lond. B Biol. Sci. 355, 1677-1684 (2000).
24. Ebert, D. Experimental evolution of parasites. Science 282, 1432-1435 (1998).
25. Elena, S. F. Restrictions to RNA virus adaptation: an experimental approach. Antonie van Leeuwenhoek 81, 135-142 (2002).
26. Bull, J. J. et al. Exceptional convergent evolution in a virus. Genetics 147, 1497-1507 (1997).
27. Cuevas, J. M., Elena, S. F. & Moya, A. molecular basis of adaptive convergence in experimental populations of RNA viruses. Genetics 162, 533-542 (2002).
28. Badgett, M. R., Auer, A., Carmichael, L. E., Parrish, C. R. & Bull, J. J. Evolutionary dynamics of viral attenuation. J. Virol. 76, 10524-10529 (2002).
29. Rokyta, D., Badgett, M. R., Molineux, I. J. & Bull, J. J. Experimental genomic evolution: extensive compensation for loss of DNA ligase activity in a virus. Mol. Biol. Evol. 19, 230-238 (2002).
30. Elena, S. F. & Moya, A. Rate of deleterious mutation and the distribution of its effects on fitness in vesicular stomatitis virus. J. Evol. Biol. 12, 1078-1088 (1999).
31. Chao, L., Rang, C. U. & Wong, L. E. Distribution of spontaneous mutants and inferences about the replication mode of the RNA bacteriophage φ6. J. Virol. 76, 3276-3281 (2002).
32. Wahl, L. M., Gerrish, P. J. & Saika-Voivod, I. Evaluating the impact of population bottlenecks in experimental evolution. Genetics 162, 961-971 (2002).
33. Lazaro, E., Escarmis, C., Perez-Mercader, J., Manrubia, S. C. & Domingo, E. 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 (2003).
34. Miralles, R., Gerrish, P. J., Moya, A. & Elena, S. F. Clonal interference and the evolution of RNA viruses. Science 285, 1745-1747 (1999).
35. Novella, I. S. Contributions of vesicular stomatitis virus to the understanding of RNA virus evolution. Curr. Opin. Microbiol. 6, 399-405 (2003).
36. Wahl, L. M. & Krakauer, D. C. Models of experimental evolution: the role of genetic chance and selective necessity. Genetics 156, 1437-1448 (2000).
37. Chao, L. Fitness of RNA virus decreased by Muller's ratchet. Nature 348, 454-455 (1990).
38. de la Peña, M., Elena, S. F. & Moya, A. Effect of deleterious mutation-accumulation on the fitness of RNA bacteriophage MS2. Evolution 54, 686-691 (2000).
39. Fraile, A. et al. Genetic exchange by recombination or reassortment is infrequent in natural populations of a tripartite RNA plant virus. J. Virol. 71, 934-940 (1997).
40. Chao, L., Tran, T. T. & Tran, T. T. The advantage of sex in the RNA virus φ6. Genetics 147, 953-959 (1997).
41. Elena, S. F. et al. Evolutionary dynamics of fitness recovery from the debilitating effects of Muller's ratchet. Evolution 52, 309-314 (1998).
42. Chao, L. Evolution of sex and the molecular clock in RNA viruses. Gene 205, 301-308 (1997).
43. Clarke, D. K. et al. The red queen reigns in the kingdom of RNA viruses. Proc. Natl Acad. Sci. USA 91, 4821-4824 (1994).
44. Wichman, H. A., Badgett, M. R., Scott, L. A., Boulianne, C. M. & Bull, J. J. Different trajectories of parallel evolution during viral adaptation. Science 285, 422-424 (1999).
45. Gerrish, P. J. The rhythm of microbial adaptation. Nature 413, 299-302 (2001).
46. Turner, P. E. & Chao, L. Prisoner's dilemma in an RNA virus. Nature 398, 441-443 (1999).
47. Turner, P. E. & Chao, L. Escape from prisoner's dilemma in RNA phage φ. Am. Nat. 161, 497-505 (2003).
48. Wilke, C. O. & Adami, C. The biology of digital organisms. Trends Ecol. Evol. 17, 528-532 (2002).
49. Yedid, G. & Bell, G. Microevolution in an electronic microcosm. Am. Nat. 157, 465-487 (2001).
50. Yedid, G. & Bell, G. Macroevolution simulated with autonomously replicating computer programs. Nature 420, 810-812 (2002).
51. Lenski, R. E., Ofria, C., Collier, T. C. & Adami, C. Genome complexity, robustness and genetic interactions in digital organisms. Nature 400, 661-664 (1999).
52. Wilke, C. O., Wang, J. L., Ofria, C., Lenski, R. E. & Adami, C. Evolution of digital organisms at high mutation rates leads to survival of the flattest. Nature 412, 331-333 (2001).
53. Kilbourne, E. D. The molecular epidemiology of influenza. J. Infect. Dis. 127, 478-487 (1973).
54. Holmes, E. C., Zhang, L. Q., Simmonds, P., Ludlam, C. A. & Brown, A. J. Convergent and divergent sequence evolution in the surface envelope glycoprotein of human immunodeficiency virus type 1 within a single infected patient. Proc. Natl Acad. Sci. USA 89, 4835-4839 (1992).
55. Scott, T. W., Weaver, S. C. & Mallampalli, V. L. in The Evolutionary Biology of Viruses (ed. Morse, S. S.) 293-324 (Raven Press, New York, 1994).
56. Rosenberg, N. A. & Nordborg, M. Genealogical trees, coalescent theory and the analysis of genetic polymorphisms. Nature Rev. Genet. 3, 380-390 (2002).
57. Drummond, A. J., Pybus, O. G., Rambaut, A., Forsberg, R. & Rodrigo, A. G. Measurably evolving populations. Trends Ecol. Evol. 18, 481-488 (2003).
58. Shankarappa, R. et al. Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J. Virol. 73, 10489-10502 (1999).
59. Drummond, A. J., Nicholls, G. K., Rodrigo, A. G. & Solomon, W. Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161, 1307-1320 (2002).
60. Drummond, A., Forsberg, R. & Rodrigo, A. G. The inference of stepwise changes in substitution rates using serial sequence samples. Mol. Biol. Evol. 18, 1365-1371 (2001).
61. Seo, T. K., Thorne, J. L., Hasegawa, M. & Kishino, H. A viral sampling design for testing the molecular clock and for estimating evolutionary rates and divergence times. Bioinformatics 18, 115-123 (2002).
62. Kingman, J. F. C. On the genealogy of large populations. J. Appl. Prob. 19, 27-43 (1982).
63. Tajima, F. Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437-460 (1983).
64. Hudson, R. R. Properties of a neutral allele model with intragenic recombination. Theor. Pop. Biol. 23, 183-201 (1983).
65. Marra, M. A. et al. The genome sequence of the SARS-associated coronavirus. Science 300, 1399-1404 (2003).
66. Robbins, K. E. et al. US human immunodeficiency virus type 1 epidemic: date of origin, population history, and characterization of early strains. J. Virol. 77, 6359-6366 (2003).
67. Lemey, P. et al. Tracing the orgin and history of the HIV-2 epidemic. Proc. Natl Acad. Sci. USA 100, 6588-6592 (2003).
68. Ou, C. Y. et al. Molecular epidemiology of HIV transmission in a dental practice. Science 256, 1165-1171 (1992).
69. Albert, J., Wahlberg, J., Leitner, T., Escanilla, D. & Uhlen, M. Analysis of a rape case by direct sequencing of the human immunodeficiency virus type 1 pol and gag genes. J. Virol. 68, 5918-5924 (1994).
70. Power, J. P. et al. Molecular epidemiology of an outbreak of infection with hepatitis C virus in recipients of anti-D immunoglobulin. Lancet 345, 1211-1213 (1995).
71. Esteban, J. I. et al. Transmission of hepatitis C virus by a cardiac surgeon. N. Engl. J. Med. 334, 555-560 (1996).
72. Ross, H. A. & Rodrigo, A. G. Immune-mediated positive selection drives human immunodeficiency virus type 1 molecular variation and predicts disease duration. J. Virol. 76, 11715-11720 (2002).
73. Nielsen, R. & Yang, Z. Likelihood model for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148, 929-936 (1998).
74. Holmes, E. C. Patterns of intra- and interhost nonsynonymous variation reveal strong purifying selection in dengue virus. J. Virol. 77, 11296-11298 (2003).
75. Costa-Mattioli, M. et al. Evidence of recombination in natural populations of hepatitis A virus. Virology 311, 51-59 (2003).
76. Kalinina, O., Norder, H., Mukomolov, S. & Magnius, L. O. A natural intergenotypic recombinant of hepatitis C virus identified in St Petersburg. J. Virol. 76, 4034-4043 (2002).
77. Korber, B. et al. Timing the ancestor of the HIV-1 pandemic strains. Science 288, 1789-1796 (2000).
78. Pavesi, A. Origin and evolution of GBV-C/hepatitis G virus and relationships with ancient human migrations. J. Mol. Evol. 53, 104-113 (2001).
79. Pybus, O. G., Rambaut, A. & Harvey, P. H. An integrated framework for the inference of viral population history from reconstructed genealogies. Genetics 155, 1429-1437 (2000).
80. Pybus, O. G. et al. The epidemic behavior of the hepatitis C virus. Science 292, 2323-2325 (2001).
81. Tanaka, Y. et al. A comparison of the molecular clock of hepatitis C virus in the United States and Japan predicts that hepatocellular carcinoma incidence in the United States will increase over the next two decades. Proc. Natl Acad. Sci. USA 99, 15584-15589 (2002).
82. Jenkins, G. M., Rambaut, A., Pybus, O. G. & Holmes, E. C. Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J. Mol. Evol. 54, 156-165 (2002).
83. Salemi, M. et al. Different population dynamics of human T-cell lymphotropic virus type II in intravenous drug users compared with endemically infected tribes. Proc. Natl Acad. Sci. USA 96, 13253-13258 (1999).
84. Buonagurio, D. A. et al. Evolution of human influenza A viruses over 50 years: rapid, uniform rate of change in NS gene. Science 232, 930-932 (1986).
85. Gillespie, J. H. Episodic evolution of RNA viruses. Proc. Natl Acad. Sci. USA 90, 10411-11041 (1993).
86. Nichol, S. T., Rowe, J. E. & Fitch, W. M. Punctuated equilibrium and positive Darwinian evolution in vesicular stomatitis virus. Proc. Natl Acad. Sci. USA 90, 10424-11042 (1993).
87. Li, W. H., Tanimura, M. & Sharp, P. M. Rates and dates of divergence between AIDS virus nucleotide sequences. Mol. Biol. Evol. 5, 313-330 (1988).
88. Overbaugh, J. & Bangham, C. R. M. Selection forces and constraints on retroviral sequence variation. Science 292, 1106-1109 (2001).
89. Holmes, E. C. Molecular clocks and the puzzle of RNA virus origins. J. Virol. 77, 3893-3897 (2003).
90. Plyusnin, A. & Morzunov, S. P. Virus evolution and genetic diversity of hantaviruses and their rodent hosts. Curr. Top. Microbiol. Immunol. 256, 47-75 (2001).
91. McGeoch, D. J., Dolan, A. & Ralph, A. C. Toward a comprehensive phylogeny for mammalian and avian herpesviruses. J. Virol. 74, 10401-10406 (2000).
92. Daszak, P., Cunningham, A. A. & Hyatt, A. D. Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 287, 443-449 (2000).
93. Morse, S. S. Factors in the emergence of infectious diseases. Emerg. Infect. Dis. 1, 7-15 (1995).
94. Cleaveland, S., Laurenson, M. K. & Taylor, L. H. Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Philos. Trans R. Soc. Lond. B Biol. Sci. 356, 991-999 (2001).
95. Woolhouse, M. E. J., Taylor, L. H. & Haydon, D. T. Population biology of multihost pathogens. Science 292, 1109-1112 (2001).
96. Holmes, E. C. Error thresholds and the constraints to RNA virus evolution. Trends Microbiol. 11, 543-546 (2003).
97. Woelk, C. H. & Holmes, E. C. Reduced positive selection in vector-borne RNA viruses. Mol. Biol. Evol. 19, 2333-2336 (2002).
98. Defilippis, V. R. & Villarreal, L. P. in Viral Ecology (ed. Hurst, C. J.) 126-208 (Academic Press, New York, 2000).
99. Baranowski, E., Ruiz-Jarabo, C. M. & Domingo, E. Evolution of cell recognition by viruses. Science 292, 1102-1105 (2001).
100. Scholtissek, C., Ludwig, S. & Fitch, W. M. Analysis of influenza A virus nucleoproteins for the assessment of molecular genetic mechanisms leading to new phylogenetic virus lineages. Arch. Virol. 131, 237-250 (1993).
101. Peeters, M. et al. Risk to human health from a plethora of simian immunodeficiency viruses in primate bushmeat. Emerg. Infect. Dis. 8, 451-457 (2002).
102. Gao, F. et al. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397, 436-441 (1999).
103. Hahn, B. H., Shaw, G. M., de Cock, K. M. & Sharp, P. M. AIDS as a zoonosis: scientific and public health implications. Science 287, 607-614 (2000).
104. Charleston, M. A. & Robertson, D. L. Preferential host switching by primate lentiviruses can account for phylogenetic similarity with the primate phylogeny. Syst. Biol. 51, 528-535 (2002).
105. Rota, P. A. et al. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300, 1394-1399 (2003).
106. Eickmann, M. et al. Phylogeny of the SARS coronavirus. Science 302, 1504-1505 (2003).
107. Guan, Y. et al. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302, 276-278 (2003).
108. Stavrinides, J. & Guttman, D. S. Mosaic evolution of the severe acute respiratory syndrome coronavirus. J. Virol. 78, 76-82 (2004).
109. Bush, R. M., Bender, C. A., Subbarao, K., Cox, N. J. & Fitch, W. M. Predicting the evolution of human influenza A. Science 286 1921-1925 (1999).
110. Anderson, R. M. & May, R. M. Infectious Diseases of Humans (Oxford Univ. Press, Oxford, 1991).
111. Culley, A. I., Lang, A. S. & Suttle, C. A. High diversity of unknown picorna-like viruses in the sea. Nature 424, 1054-1057 (2003).
112. Levin, S. A. & Andreasen, V. Disease transmission dynamics and the evolution of antibiotic resistance in hospitals and communal settings. Proc. Natl Acad. Sci. USA 96, 800-801 (1999).
113. Levin, B. R., Lipsitch, M., & Bonhoeffer, S. Population biology, evolution, and infectious disease: convergence and synthesis. Science 283, 806-809 (1999).
114. Wain-Hobson, S. Down or out in blood and lymph? Nature 387, 123-124 (1997).
115. Wong, J. K. et al. Recovery of replication-competent HIV despite prolonged suppression of plasma viremia. Science 278 1291-1295 (1997).
116. Jung, A. et al. Recombination: multiply infected spleen cells in HIV patients. Nature 418, 144 (2002).
117. Bonhoeffer, S., May, R. M., Shaw, G. M. & Nowak, M. A. Virus dynamics and drug therapy. Proc. Natl Acad. Sci. USA 94, 6971-6976 (1997).
118. Back, N. K. et al. Reduced replication of 3TC-resistant HIV-1 variants in primary cells due to a processivity defect of the reverse transcriptase enzyme. EMBO J. 15, 4040-4049 (1996).
119. Simon, V. et al. Infectivity and replication capacity of drug-resistant human immunodeficiency virus type 1 variants isolated during primary infection. J. Virol. 77, 7736-7745 (2003).
120. Pitisuttithum, P. et al. Safety and immunogenicity of combinations of recombinant subtype E and B human immunodeficiency virus type 1 envelope glycoprotein 120 vaccines in healthy Thai adults. J. Infect. Dis. 188, 219-227 (2003).
121. Fitch, W. M., Leiter, J. M. E., Li, X. Q. & Pease, P. Positive Darwinian evolution in human influenza-A viruses. Proc. Natl Acad. Sci. USA 88, 4270-4274 (1991).
122. Yusim, K. et al. Clustering patterns of cytotoxic T-lymphocyte epitopes in human immunodeficiency virus type 1 (HIV-1) proteins reveal imprints of immune evasion on HIV-1 global variation. J. Virol. 76, 8757-8768 (2002).
123. Moore, C. B. et al. Evidence for HIV-1 adaptation to HLA-restricted immune responses at the population level. Science 296, 1439-1443 (2002).
124. Wei, X. et al. Antibody neutralization and escape by HIV-1. Nature 422, 307-312 (2003).
125. Grassly, N. C., Harvey, P. H. & Holmes, E. C. Population dynamics of HIV-1 inferred from gene sequences. Genetics 151, 427-438 (1999).
126. Delwart, E. et al. Homogeneous quasispecies in 16 out of 17 individuals during very early HIV-1 primary infection. AIDS 16, 189-195 (2002).
127. Lipsitch, M. & Moxon, E. R. Virulence and transmissibility of pathogens: what is the relationship? Trends Microbiol. 5, 31-37 (1997).
128. Ebert, D. & Bull, J. J. Challenging the trade-off model for the evolution of virulence: is virulence management feasible? Trends Microbiol. 11, 15-20 (2003).
129. Bergstrom, C. T., McElhany, P. & Real, L. A. Transmission bottlenecks as determinants of virulence in rapidly evolving pathogens. Proc. Natl Acad. Sci. USA 96, 5095-5100 (1999).
130. Nowak, M. A. & May, R. M. Superinfection and the evolution of parasite virulence. Proc. R. Soc. Lond. B Biol. Sci. 255, 81-89 (1994).
131. Zhang, L. et al. Chemokine coreceptor usage by diverse primary isolates of human immunodeficiency virus type 1. J. Virol. 72, 9307-9312 (1998).
132. Zhu, T. et al. Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science 261, 1179-1181 (1993).
133. Metzker, M. L. et al. Molecular evidence of HIV-1 transmission in a criminal case. Proc. Natl Acad. Sci. USA 99 14292-14297 (2002).
134. González-Candelas, F., Bracho, M. A. & Moya, A. Molecular epidemiology and forensic genetics: application to a hepatitis C virus transmission event at a hemodialysis unit. J. Infect. Dis. 187 352-358 (2003).
135. Strimmer, K. & von Haeseler, A. Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13, 964-969 (1996).
136. Swofford, D. L. PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. (Sinauer Associates, Sunderland, Massachusetts, 2002).