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Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2001 Nov 22;268(1483):2331–2337. doi: 10.1098/rspb.2001.1795

Interactions between sources of mortality and the evolution of parasite virulence.

P D Williams 1, T Day 1
PMCID: PMC1088884  PMID: 11703873

Abstract

A well-known result from the theory of the evolution of virulence is the prediction that the virulence of a pathogen (i.e. the rate of parasite-induced host mortality) always evolves to higher levels when host background mortality rates increase. This prediction, however, is derived from models that assume that host mortality sources combine additively to determine the overall host mortality rate. In this paper, we suggest that such additivity is probably rare for many host-pathogen systems, and explore how the predictions for the evolution of virulence are altered when interactions between host mortality sources are incorporated into the theory. Our results indicate that if mortality-source interactions are sufficiently strong then the evolutionarily stable level of virulence can actually decrease as the background mortality rate increases. Consequently, a detailed mechanistic description of how parasites and other mortality sources combine to cause host mortality is required before reliable predictions about virulence evolution can be made. Moreover, mortality-source interactions make empirical comparisons of the virulence of different parasites a much more subtle issue.

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Selected References

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  1. Anderson R. M., May R. M. Coevolution of hosts and parasites. Parasitology. 1982 Oct;85(Pt 2):411–426. doi: 10.1017/s0031182000055360. [DOI] [PubMed] [Google Scholar]
  2. Anderson R. M., May R. M. Population biology of infectious diseases: Part I. Nature. 1979 Aug 2;280(5721):361–367. doi: 10.1038/280361a0. [DOI] [PubMed] [Google Scholar]
  3. Bonifassi E., Fischer-Le Saux M., Boemare N., Lanois A., Laumond C., Smart G. Gnotobiological study of infective juveniles and symbionts of Steinernema scapterisci: A model to clarify the concept of the natural occurrence of monoxenic associations in entomopathogenic nematodes. J Invertebr Pathol. 1999 Sep;74(2):164–172. doi: 10.1006/jipa.1999.4866. [DOI] [PubMed] [Google Scholar]
  4. Diekmann O., Heesterbeek J. A., Metz J. A. On the definition and the computation of the basic reproduction ratio R0 in models for infectious diseases in heterogeneous populations. J Math Biol. 1990;28(4):365–382. doi: 10.1007/BF00178324. [DOI] [PubMed] [Google Scholar]
  5. Dobson A. P. The population biology of parasite-induced changes in host behavior. Q Rev Biol. 1988 Jun;63(2):139–165. doi: 10.1086/415837. [DOI] [PubMed] [Google Scholar]
  6. Ebert D., Herre E. A. The evolution of parasitic diseases. Parasitol Today. 1996 Mar;12(3):96–101. doi: 10.1016/0169-4758(96)80668-5. [DOI] [PubMed] [Google Scholar]
  7. Ebert D. Virulence and local adaptation of a horizontally transmitted parasite. Science. 1994 Aug 19;265(5175):1084–1086. doi: 10.1126/science.265.5175.1084. [DOI] [PubMed] [Google Scholar]
  8. Ebert D., Weisser W. W. Optimal killing for obligate killers: the evolution of life histories and virulence of semelparous parasites. Proc Biol Sci. 1997 Jul 22;264(1384):985–991. doi: 10.1098/rspb.1997.0136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ehlers R. U., Wulff A., Peters A. Pathogenicity of axenic Steinernema feltiae, Xenorhabdus bovienii, and the bacto-helminthic complex to larvae of Tipula oleracea (Diptera) and Galleria mellonella (Lepidoptera). J Invertebr Pathol. 1997 May;69(3):212–217. doi: 10.1006/jipa.1996.4647. [DOI] [PubMed] [Google Scholar]
  10. Frank S. A. Models of parasite virulence. Q Rev Biol. 1996 Mar;71(1):37–78. doi: 10.1086/419267. [DOI] [PubMed] [Google Scholar]
  11. Gulland F. M. The role of nematode parasites in Soay sheep (Ovis aries L.) mortality during a population crash. Parasitology. 1992 Dec;105(Pt 3):493–503. doi: 10.1017/s0031182000074679. [DOI] [PubMed] [Google Scholar]
  12. Herre E. A. Population structure and the evolution of virulence in nematode parasites of fig wasps. Science. 1993 Mar 5;259(5100):1442–1445. doi: 10.1126/science.259.5100.1442. [DOI] [PubMed] [Google Scholar]
  13. Imhoof B., Schmid-Hempel P. Single-clone and mixed-clone infections versus host environment in Crithidia bombi infecting bumblebees. Parasitology. 1998 Oct;117(Pt 4):331–336. doi: 10.1017/s0031182098003138. [DOI] [PubMed] [Google Scholar]
  14. Karyeija R. F., Kreuze J. F., Gibson R. W., Valkonen J. P. Synergistic interactions of a potyvirus and a phloem-limited crinivirus in sweet potato plants. Virology. 2000 Mar 30;269(1):26–36. doi: 10.1006/viro.1999.0169. [DOI] [PubMed] [Google Scholar]
  15. Latham M. C. Nutrition and infection in national development. Science. 1975 May 9;188(4188):561–565. doi: 10.1126/science.1124393. [DOI] [PubMed] [Google Scholar]
  16. Lenski R. E. Evolution of plague virulence. Nature. 1988 Aug 11;334(6182):473–474. doi: 10.1038/334473a0. [DOI] [PubMed] [Google Scholar]
  17. Lenski R. E., May R. M. The evolution of virulence in parasites and pathogens: reconciliation between two competing hypotheses. J Theor Biol. 1994 Aug 7;169(3):253–265. doi: 10.1006/jtbi.1994.1146. [DOI] [PubMed] [Google Scholar]
  18. Lipsitch M., Moxon E. R. Virulence and transmissibility of pathogens: what is the relationship? Trends Microbiol. 1997 Jan;5(1):31–37. doi: 10.1016/S0966-842X(97)81772-6. [DOI] [PubMed] [Google Scholar]
  19. May R. M., Anderson R. M. Epidemiology and genetics in the coevolution of parasites and hosts. Proc R Soc Lond B Biol Sci. 1983 Oct 22;219(1216):281–313. doi: 10.1098/rspb.1983.0075. [DOI] [PubMed] [Google Scholar]
  20. May R. M., Anderson R. M. Parasite-host coevolution. Parasitology. 1990;100 (Suppl):S89–101. doi: 10.1017/s0031182000073042. [DOI] [PubMed] [Google Scholar]
  21. Messenger S. L., Molineux I. J., Bull J. J. Virulence evolution in a virus obeys a trade-off. Proc Biol Sci. 1999 Feb 22;266(1417):397–404. doi: 10.1098/rspb.1999.0651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Poulin R., Combes C. The concept of virulence: interpretations and implications. Parasitol Today. 1999 Dec;15(12):474–475. doi: 10.1016/s0169-4758(99)01554-9. [DOI] [PubMed] [Google Scholar]
  23. Read A. F. The evolution of virulence. Trends Microbiol. 1994 Mar;2(3):73–76. doi: 10.1016/0966-842x(94)90537-1. [DOI] [PubMed] [Google Scholar]
  24. Slater A. F., Keymer A. E. The influence of protein deficiency on immunity to Heligmosomoides polygyrus (Nematoda) in mice. Parasite Immunol. 1988 Sep;10(5):507–522. doi: 10.1111/j.1365-3024.1988.tb00239.x. [DOI] [PubMed] [Google Scholar]
  25. Vance V. B. Replication of potato virus X RNA is altered in coinfections with potato virus Y. Virology. 1991 Jun;182(2):486–494. doi: 10.1016/0042-6822(91)90589-4. [DOI] [PubMed] [Google Scholar]

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