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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2004 Jul 29;359(1447):1059–1065. doi: 10.1098/rstb.2004.1478

Viral evolution and the emergence of SARS coronavirus.

Edward C Holmes 1, Andrew Rambaut 1
PMCID: PMC1693395  PMID: 15306390

Abstract

The recent appearance of severe acute respiratory syndrome coronavirus (SARS-CoV) highlights the continual threat to human health posed by emerging viruses. However, the central processes in the evolution of emerging viruses are unclear, particularly the selection pressures faced by viruses in new host species. We outline some of the key evolutionary genetic aspects of viral emergence. We emphasize that, although the high mutation rates of RNA viruses provide them with great adaptability and explain why they are the main cause of emerging diseases, their limited genome size means that they are also subject to major evolutionary constraints. Understanding the mechanistic basis of these constraints, particularly the roles played by epistasis and pleiotropy, is likely to be central in explaining why some RNA viruses are more able than others to cross species boundaries. Viral genetic factors have also been implicated in the emergence of SARS-CoV, with the suggestion that this virus is a recombinant between mammalian and avian coronaviruses. We show, however, that the phylogenetic patterns cited as evidence for recombination are more probably caused by a variation in substitution rate among lineages and that recombination is unlikely to explain the appearance of SARS in humans.

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Selected References

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  1. Baranowski E., Ruiz-Jarabo C. M., Domingo E. Evolution of cell recognition by viruses. Science. 2001 May 11;292(5519):1102–1105. doi: 10.1126/science.1058613. [DOI] [PubMed] [Google Scholar]
  2. Charleston M. A., Robertson D. L. Preferential host switching by primate lentiviruses can account for phylogenetic similarity with the primate phylogeny. Syst Biol. 2002 Jun;51(3):528–535. doi: 10.1080/10635150290069940. [DOI] [PubMed] [Google Scholar]
  3. 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. 2001 Jul 29;356(1411):991–999. doi: 10.1098/rstb.2001.0889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Crotty S., Cameron C. E., Andino R. RNA virus error catastrophe: direct molecular test by using ribavirin. Proc Natl Acad Sci U S A. 2001 May 22;98(12):6895–6900. doi: 10.1073/pnas.111085598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cuevas José M., Elena Santiago F., Moya Andrés. Molecular basis of adaptive convergence in experimental populations of RNA viruses. Genetics. 2002 Oct;162(2):533–542. doi: 10.1093/genetics/162.2.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Culley Alexander I., Lang Andrew S., Suttle Curtis A. High diversity of unknown picorna-like viruses in the sea. Nature. 2003 Aug 28;424(6952):1054–1057. doi: 10.1038/nature01886. [DOI] [PubMed] [Google Scholar]
  7. Daubin Vincent, Moran Nancy A., Ochman Howard. Phylogenetics and the cohesion of bacterial genomes. Science. 2003 Aug 8;301(5634):829–832. doi: 10.1126/science.1086568. [DOI] [PubMed] [Google Scholar]
  8. Drake J. W., Charlesworth B., Charlesworth D., Crow J. F. Rates of spontaneous mutation. Genetics. 1998 Apr;148(4):1667–1686. doi: 10.1093/genetics/148.4.1667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eickmann Markus, Becker Stephan, Klenk Hans-Dieter, Doerr Hans Wilhelm, Stadler Konrad, Censini Stefano, Guidotti Silvia, Masignani Vega, Scarselli Maria, Mora Marirosa. Phylogeny of the SARS coronavirus. Science. 2003 Nov 28;302(5650):1504–1505. doi: 10.1126/science.302.5650.1504b. [DOI] [PubMed] [Google Scholar]
  10. Eigen M. New concepts for dealing with the evolution of nucleic acids. Cold Spring Harb Symp Quant Biol. 1987;52:307–320. doi: 10.1101/sqb.1987.052.01.036. [DOI] [PubMed] [Google Scholar]
  11. Eigen M. On the nature of virus quasispecies. Trends Microbiol. 1996 Jun;4(6):216–218. doi: 10.1016/0966-842X(96)20011-3. [DOI] [PubMed] [Google Scholar]
  12. Gao F., Bailes E., Robertson D. L., Chen Y., Rodenburg C. M., Michael S. F., Cummins L. B., Arthur L. O., Peeters M., Shaw G. M. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature. 1999 Feb 4;397(6718):436–441. doi: 10.1038/17130. [DOI] [PubMed] [Google Scholar]
  13. Guan Y., Zheng B. J., He Y. Q., Liu X. L., Zhuang Z. X., Cheung C. L., Luo S. W., Li P. H., Zhang L. J., Guan Y. J. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science. 2003 Sep 4;302(5643):276–278. doi: 10.1126/science.1087139. [DOI] [PubMed] [Google Scholar]
  14. Hahn B. H., Shaw G. M., De Cock K. M., Sharp P. M. AIDS as a zoonosis: scientific and public health implications. Science. 2000 Jan 28;287(5453):607–614. doi: 10.1126/science.287.5453.607. [DOI] [PubMed] [Google Scholar]
  15. Hillis D. M. Inferring complex phylogenies. Nature. 1996 Sep 12;383(6596):130–131. doi: 10.1038/383130a0. [DOI] [PubMed] [Google Scholar]
  16. Holmes Edward C. Error thresholds and the constraints to RNA virus evolution. Trends Microbiol. 2003 Dec;11(12):543–546. doi: 10.1016/j.tim.2003.10.006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Holmes Edward C. The phylogeography of human viruses. Mol Ecol. 2004 Apr;13(4):745–756. doi: 10.1046/j.1365-294x.2003.02051.x. [DOI] [PubMed] [Google Scholar]
  18. Kishino H., Hasegawa M. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J Mol Evol. 1989 Aug;29(2):170–179. doi: 10.1007/BF02100115. [DOI] [PubMed] [Google Scholar]
  19. Malpica José M., Fraile Aurora, Moreno Ignacio, Obies Clara I., Drake John W., García-Arenal Fernando. The rate and character of spontaneous mutation in an RNA virus. Genetics. 2002 Dec;162(4):1505–1511. doi: 10.1093/genetics/162.4.1505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Marra Marco A., Jones Steven J. M., Astell Caroline R., Holt Robert A., Brooks-Wilson Angela, Butterfield Yaron S. N., Khattra Jaswinder, Asano Jennifer K., Barber Sarah A., Chan Susanna Y. The Genome sequence of the SARS-associated coronavirus. Science. 2003 May 1;300(5624):1399–1404. doi: 10.1126/science.1085953. [DOI] [PubMed] [Google Scholar]
  21. McLysaght Aoife, Hokamp Karsten, Wolfe Kenneth H. Extensive genomic duplication during early chordate evolution. Nat Genet. 2002 May 28;31(2):200–204. doi: 10.1038/ng884. [DOI] [PubMed] [Google Scholar]
  22. Morse S. S. Factors in the emergence of infectious diseases. Emerg Infect Dis. 1995 Jan-Mar;1(1):7–15. doi: 10.3201/eid0101.950102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rest Joshua S., Mindell David P. SARS associated coronavirus has a recombinant polymerase and coronaviruses have a history of host-shifting. Infect Genet Evol. 2003 Sep;3(3):219–225. doi: 10.1016/j.meegid.2003.08.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sanz AI, Fraile A, Gallego JM, Malpica JM, Garcia-Arenal F. Genetic variability of natural populations of cotton leaf curl geminivirus, a single-stranded DNA virus. J Mol Evol. 1999 Nov;49(5):672–681. doi: 10.1007/pl00006588. [DOI] [PubMed] [Google Scholar]
  25. Schliekelman P., Garner C., Slatkin M. Natural selection and resistance to HIV. Nature. 2001 May 31;411(6837):545–546. doi: 10.1038/35079176. [DOI] [PubMed] [Google Scholar]
  26. Sierra S., Dávila M., Lowenstein P. R., Domingo E. Response of foot-and-mouth disease virus to increased mutagenesis: influence of viral load and fitness in loss of infectivity. J Virol. 2000 Sep;74(18):8316–8323. doi: 10.1128/jvi.74.18.8316-8323.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Simmonds P. Variability of hepatitis C virus. Hepatology. 1995 Feb;21(2):570–583. doi: 10.1002/hep.1840210243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Stanhope Michael J., Brown James R., Amrine-Madsen Heather. Evidence from the evolutionary analysis of nucleotide sequences for a recombinant history of SARS-CoV. Infect Genet Evol. 2004 Mar;4(1):15–19. doi: 10.1016/j.meegid.2003.10.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Stavrinides John, Guttman David S. Mosaic evolution of the severe acute respiratory syndrome coronavirus. J Virol. 2004 Jan;78(1):76–82. doi: 10.1128/JVI.78.1.76-82.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Turner P. E., Elena S. F. Cost of host radiation in an RNA virus. Genetics. 2000 Dec;156(4):1465–1470. doi: 10.1093/genetics/156.4.1465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Whelan S., Goldman N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol. 2001 May;18(5):691–699. doi: 10.1093/oxfordjournals.molbev.a003851. [DOI] [PubMed] [Google Scholar]
  32. Woelk Christopher H., Holmes Edward C. Reduced positive selection in vector-borne RNA viruses. Mol Biol Evol. 2002 Dec;19(12):2333–2336. doi: 10.1093/oxfordjournals.molbev.a004059. [DOI] [PubMed] [Google Scholar]
  33. Woolhouse M. E., Taylor L. H., Haydon D. T. Population biology of multihost pathogens. Science. 2001 May 11;292(5519):1109–1112. doi: 10.1126/science.1059026. [DOI] [PubMed] [Google Scholar]
  34. Worobey M., Holmes E. C. Evolutionary aspects of recombination in RNA viruses. J Gen Virol. 1999 Oct;80(Pt 10):2535–2543. doi: 10.1099/0022-1317-80-10-2535. [DOI] [PubMed] [Google Scholar]
  35. Worobey Michael, Rambaut Andrew, Pybus Oliver G., Robertson David L. Questioning the evidence for genetic recombination in the 1918 "Spanish flu" virus. Science. 2002 Apr 12;296(5566):211–211. doi: 10.1126/science.296.5566.211a. [DOI] [PubMed] [Google Scholar]

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