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. 2007;315:51–66. doi: 10.1007/978-3-540-70962-6_3

The Evolutionary Genetics of Viral Emergence

E C Holmes 8, A J Drummond 9
Editors: James E Childs5, John S Mackenzie6, Jürgen A Richt7
PMCID: PMC7120214  PMID: 17848060

Abstract

Despite the wealth of data describing the ecological factors that underpin viral emergence, little is known about the evolutionary processes that allow viruses to jump species barriers and establish productive infections in new hosts. Understanding the evolutionary basis to virus emergence is therefore a key research goal and many of the debates in this area can be considered within the rigorous theoretical framework established by evolutionary genetics. In particular, the respective roles played by natural selection and genetic drift in shaping genetic diversity are also of fundamental importance for understanding the nature of viral emergence. Herein, we discuss whether there are evolutionary rules to viral emergence, and especially whether certain types of virus, or those that infect a particular type of host species, are more likely to emerge than others. We stress the complex interplay between rates of viral evolution and the ability to recognize cell receptors from phylogenetically divergent host species. We also emphasize the current lack of convincing data as to whether viral emergence requires adaptation to the new host species during the early stages of infection, or whether it is largely a chance process involving the transmission of a viral strain with the necessary genetic characteristics.

Keywords: Avian Influenza, Dengue Virus, Severe Acute Respiratory Syndrome, Viral Emergence, Yellow Fever Virus

Contributor Information

James E. Childs, Email: Jamesechilds@comcast.net

John S. Mackenzie, Email: J.Mackenzie@curtin.edu.au

Jürgen A. Richt, Email: juergen.richt@ars.usda.gov

E. C. Holmes, Email: ech15@psu.edu

A. J. Drummond, Email: alexei@cs.auckland.ac.nz

References

  1. Antia R, Regoes RR, Koella JC, Bergstrom CT. The role of evolution in the emergence of infectious diseases. Nature. 2003;426:658–610. doi: 10.1038/nature02104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bailes E, Gao F, Bibollet-Ruche F, Courgnaud V, Peeters M, Marx PA, Hahn BH, Sharp PM. Hybrid origin of SIV in chimpanzees. Science. 2003;300:1713. doi: 10.1126/science.1080657. [DOI] [PubMed] [Google Scholar]
  3. Baranowski E, Ruiz-Jarabo CM, Domingo E. Evolution of cell recognition by viruses. Science. 2001;292:1102–1105. doi: 10.1126/science.1058613. [DOI] [PubMed] [Google Scholar]
  4. Brault AC, Powers AM, Holmes EC, Woelk CH, Weaver SC. Positively charged amino acid substitutions in the E2 envelope glycoprotein are associated with the emergence of Venezuelan equine encephalitis virus. J Virol. 2002;76:1718–1730. doi: 10.1128/JVI.76.4.1718-1730.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Breman JG, Johnson KM, van der Groen G, Robbins CB, Szczeniowski MV, Ruti K, Webb PA, Meier F, Heymann DL. A search for Ebola virus in animals in the Democratic Republic of the Congo and Cameroon: ecologic, virologic, and serologic surveys, 1979–1980. J Infect Dis. 1999;179:S139–S147. doi: 10.1086/514278. [DOI] [PubMed] [Google Scholar]
  6. Chare ER, Holmes EC. Selection pressures in the capsid genes of plant RNA viruses reflect mode of transmission. J Gen Virol. 2004;85:3149–3157. doi: 10.1099/vir.0.80134-0. [DOI] [PubMed] [Google Scholar]
  7. Chare ER, Gould EA, Holmes EC. Phylogenetic analysis reveals a low rate of homologous recombination in negative-sense RNA viruses. J Gen Virol. 2003;84:2691–2703. doi: 10.1099/vir.0.19277-0. [DOI] [PubMed] [Google Scholar]
  8. Cleaveland S, Laurenson MK, Taylor LH. Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Phil Trans R Soc Lond B. 2001;356:991–999. doi: 10.1098/rstb.2001.0889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. De Filippis VR, Villarreal LP. An introduction to the evolutionary ecology of viruses. In: Hurst CJ, editor. Viral ecology. New York: Academic Press; 2000. pp. 126–208. [Google Scholar]
  10. Domingo E, Holland JJ. RNA virus mutations for fitness and survival. Ann Rev Microbiol. 1997;51:151–178. doi: 10.1146/annurev.micro.51.1.151. [DOI] [PubMed] [Google Scholar]
  11. Elena SF, Moya A. Rate of deleterious mutation and the distribution of its effects on fitness in vesicular stomatitis virus. J Evol Biol. 1999;12:1078–1088. doi: 10.1046/j.1420-9101.1999.00110.x. [DOI] [Google Scholar]
  12. Ferber D. Human diseases threaten great apes. Science. 2000;289:1277–1278. doi: 10.1126/science.289.5483.1277. [DOI] [PubMed] [Google Scholar]
  13. Figueroa F, Günther E, Klein J. MHC polymorphism pre-dating speciation. Nature. 1988;355:265–267. doi: 10.1038/335265a0. [DOI] [PubMed] [Google Scholar]
  14. Gaunt MW, Sall AA, de Lamballerie X, Falconar AKI, Dzhivanian TI, Gould EA. Phylogenetic relationships of flaviviruses correlate with their epidemiology, disease association and biogeography. J Gen Virol. 2001;82:1867–1876. doi: 10.1099/0022-1317-82-8-1867. [DOI] [PubMed] [Google Scholar]
  15. Gibbs AJ, Gibbs MJ, Armstrong JS. The phylogeny of SARS coronavirus. Arch Virol. 2004;149:621–624. doi: 10.1007/s00705-003-0244-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gillespie JH. Population genetics: a concise course. Baltimore: Johns Hopkins University Press; 1998. [Google Scholar]
  17. Holmes EC. Error thresholds and the constraints to RNA virus evolution. Trends Microbiol. 2003;11:543–546. doi: 10.1016/j.tim.2003.10.006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Holmes EC. Patterns of intra- and inter-host nonsynonymous variation reveal strong purifying selection in dengue virus. J Virol. 2003;77:11296–11298. doi: 10.1128/JVI.77.20.11296-11298.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Holmes EC. The phylogeography of human viruses. Mol Ecol. 2004;13:745–756. doi: 10.1046/j.1365-294X.2003.02051.x. [DOI] [PubMed] [Google Scholar]
  20. Holmes EC, Rambaut A. Viral evolution and the emergence of SARS coronavirus. Phil Trans R Soc Lond B. 2004;359:1059–1065. doi: 10.1098/rstb.2004.1478. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Huet T, Cheynier R, Meyerhans A, Roelants G, Wain-Hobson S. Genetic organisation of a chimpanzee lentivirus related to HIV-1. Nature. 1990;345:356–359. doi: 10.1038/345356a0. [DOI] [PubMed] [Google Scholar]
  22. Jung A, Maier R, Vartanian JP, Bocharov G, Jung V, Fischer U, Meese E, Wain-Hobson S, Meyerhans A. Recombination: multiply infected spleen cells in HIV patients. Nature. 2002;418:144. doi: 10.1038/418144a. [DOI] [PubMed] [Google Scholar]
  23. Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW, Wong BH, Wong SS, Leung SY, Chan KH, Yuen KY. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci U S A. 2005;102:14040–14045. doi: 10.1073/pnas.0506735102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, Wang H, Crameri G, Hu Z, Zhang H, Zhang J, McEachern J, Field H, Daszak P, Eaton BT, Zhang S, Wang LF. Bats are natural reservoirs of SARS-like coronaviruses. Science. 2005;310:676–679. doi: 10.1126/science.1118391. [DOI] [PubMed] [Google Scholar]
  25. Malpica MJ, Fraile A, Moreno I, Obies CI, Drake JW, García-Arenal F. The rate and character of spontaneous mutation in an RNA virus. Genetics. 2002;162:1505–1511. doi: 10.1093/genetics/162.4.1505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Markowitz M, Louie M, Hurley A, Sun E, Di Mascio M, Perelson AS, Ho DD. A novel antiviral intervention results in more accurate assessment of human immunodeficiency virus type 1 replication dynamics and T-cell decay in vivo. J Virol. 2003;77:5037–5038. doi: 10.1128/JVI.77.8.5037-5038.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Matrosovich MN, Gambaryan AS, Teneberg S, Piskarev VE, Yamnikova SS, Lvov DK, Robertson JS, Karlsson KA. Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology. 1997;233:224–234. doi: 10.1006/viro.1997.8580. [DOI] [PubMed] [Google Scholar]
  28. Moncayo AC, Fernandez Z, Ortiz D, Diallo M, Sall A, Hartman S, Davis CT, Coffey L, Mathiot CC, Tesh RB, Weaver SC. Dengue emergence and adaptation to peridomestic mosquitoes. Emerg Infect Dis. 2004;10:1790–1796. doi: 10.3201/eid1010.030846. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Morse SS. Factors in the emergence of infectious diseases. Emerg Infect Dis. 1995;1:7–15. doi: 10.3201/eid0101.950102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Moya A, Holmes EC, González-Candelas F. The population genetics and evolutionary epidemiology of RNA viruses. Nat Rev Microbiol. 2004;2:279–287. doi: 10.1038/nrmicro863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nichol ST, Spiropoulou CF, Morzunov S, Rollin PE, Ksiazek TG, Feldmann H, Sanchez A, Childs J, Zaki S, Peters CJ. Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness. Science. 1993;262:914–917. doi: 10.1126/science.8235615. [DOI] [PubMed] [Google Scholar]
  32. Ohta T. The nearly neutral theory of molecular evolution. Ann Rev Ecol Syst. 1992;23:263–286. doi: 10.1146/annurev.es.23.110192.001403. [DOI] [Google Scholar]
  33. Ohta T. Evolution by nearly-neutral mutations. Genetica. 1998;102(103):83–90. doi: 10.1023/A:1017007513825. [DOI] [PubMed] [Google Scholar]
  34. Okamoto H, Fukuda M, Tawara A, Nishizawa T, Itoh Y, Hayasaka I, Tsuda F, Tanaka T, Miyakawa Y, Mayumi M. Species-specific TT viruses and cross-species infection in nonhuman primates. J Virol. 2000;74:1132–1139. doi: 10.1128/JVI.74.3.1132-1139.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Peterson AT, Carroll DS, Mills JN, Johnson KM. Potential mammalian filovirus reservoirs. Emerg Infect Dis. 2004;10:2073–2081. doi: 10.3201/eid1012.040346. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Pugachev KV, Guirakhoo F, Ocran SW, Mitchell F, Parsons M, Penal C, Girakhoo S, Pougatcheva SO, Arroyo J, Trent DW, Monath TP. High fidelity of yellow fever virus RNA polymerase. J Virol. 2004;78:1032–1038. doi: 10.1128/JVI.78.2.1032-1038.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sanz AI, Fraile A, Gallego JM, Malpica JM, García-Arenal F. Genetic variability of natural populations of cotton leaf curl geminivirus, a single-stranded DNA virus. J Mol Evol. 1999;49:672–681. doi: 10.1007/PL00006588. [DOI] [PubMed] [Google Scholar]
  38. Scholtissek C, Ludwig S, Fitch WM. Analysis of influenza A virus nucleoproteins for the assessment of molecular genetic mechanisms leading to new phylogenetic virus lineages. Arch Virol. 1993;131:237–250. doi: 10.1007/BF01378629. [DOI] [PubMed] [Google Scholar]
  39. Shackelton LA, Parrish CR, Truyen U, Holmes EC. High rate of viral evolution associated with the emergence of canine parvoviruses. Proc Natl Acad Sci U S A. 2005;102:379–384. doi: 10.1073/pnas.0406765102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sharp PM, Bailes E, Chaudhuri RR, Rodenburg CM, Santiago MO, Hahn BH. The origins of acquired immune deficiency syndrome viruses: where and when? Phil Trans R Lond B. 2001;356:867–876. doi: 10.1098/rstb.2001.0863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Stanhope MJ, Brown JR, Amrine-Madsen H. Evidence from the evolutionary analysis of nucleotide sequences for a recombinant history of SARS-CoV Infect. Genet Evol. 2004;4:15–19. doi: 10.1016/j.meegid.2003.10.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Stavrinides J, Guttman DS. Mosaic evolution of the severe acute respiratory syndrome coronavirus. J Virol. 2004;78:76–82. doi: 10.1128/JVI.78.1.76-82.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Switzer WM, Salemi M, Shanmugam V, Gao F, Cong M-E, Kuiken C, Bhullar V, Beer B, Vallet D, Gautier-Hion A, Tooze A, Villinger F, Holmes EC, Heneine W. Ancient co-speciation of simian foamy viruses and primates. Nature. 2005;434:376–380. doi: 10.1038/nature03341. [DOI] [PubMed] [Google Scholar]
  44. Taubenberger JK, Reid AH, Lourens RM, Wang R, Jin G, Fanning TG. Characterization of the 1918 influenza virus polymerase genes. Nature. 2005;437:889–893. doi: 10.1038/nature04230. [DOI] [PubMed] [Google Scholar]
  45. Twiddy SS, Farrar JF, Chau NV, Wills B, Gould EA, Gritsun T, Lloyd G, Holmes EC. Phylogenetic relationships and differential selection pressures among genotypes of dengue-2 virus. Virology. 2002;298:63–72. doi: 10.1006/viro.2002.1447. [DOI] [PubMed] [Google Scholar]
  46. Wang E, Ni H, Xu R, Barrett ADT, Watowich SJ, Gubler DJ, Weaver SC. Evolutionary relationships of endemic/epidemic and sylvatic dengue viruses. J Virol. 2000;74:3227–3234. doi: 10.1128/JVI.74.7.3227-3234.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Whalley SA, Murray JM, Brown D, Webster GJ, Emery VC, Dusheiko GM, Perelson AS. Kinetics of acute hepatitis B virus infection in humans. J Exp Med. 2001;193:847–854. doi: 10.1084/jem.193.7.847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Webby RJ, Webster RG. Emergence of influenza A viruses. Phil Trans R Soc Lond B. 2001;356:1817–1828. doi: 10.1098/rstb.2001.0997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Woelk CH, Holmes EC. Reduced positive selection in vector-borne RNA viruses. Mol Biol Evol. 2002;19:2333–2336. doi: 10.1093/oxfordjournals.molbev.a004059. [DOI] [PubMed] [Google Scholar]
  50. Woolhouse MEJ, Taylor LH, Haydon DT. Population biology of multihost pathogens. Science. 2001;292:1109–1112. doi: 10.1126/science.1059026. [DOI] [PubMed] [Google Scholar]
  51. Woolhouse MEJ. Population biology of emerging and re-emerging pathogens. Trends Microbiol. 2002;10:S3–S7. doi: 10.1016/S0966-842X(02)02428-9. [DOI] [PubMed] [Google Scholar]
  52. Yeh S-H, Wang H-Y, Tsai C-Y, Kao C-L, Yang J-Y, Liu H-W, Su I-J, Tsai S-F, Chen D-S, Chen P-J. haracterization of severe acute respiratory syndrome coronavirus genomes in Taiwan: Molecular epidemiology and genome evolution. Proc Natl Acad Sci U S A. 2004;101:2542–2547. doi: 10.1073/pnas.0307904100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Zárate S, Novella IS. Vesicular stomatitis virus evolution during alternation between persistent Infection in insect cells and acute infection in mammalian cells Is dominated by the persistence phase. J Virol. 2004;78:12236–12242. doi: 10.1128/JVI.78.22.12236-12242.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]

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