Resistance is futile but tolerance can explain why parasites do not always castrate their hosts

Evolution

Volumn 64, Issue 2, 2010, Pages 348-357

  Best, Alex ^a   White, Andy ^b   Boots, Mike ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b HERIOT WATT UNIVERSITY   (United Kingdom)

Author keywords

Coevolution; Resistance; Sterility; Tolerance

Indexed keywords

COEVOLUTION; DISEASE RESISTANCE; FECUNDITY; GROWTH RATE; HOST-PARASITE INTERACTION; PARASITE; PATHOTYPE; TOLERANCE;

ADAPTATION; ANIMAL; ARTICLE; CASTRATION; EVOLUTION; HOST PARASITE INTERACTION; THEORETICAL MODEL;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CASTRATION; EVOLUTION; HOST-PARASITE INTERACTIONS; MODELS, THEORETICAL;

EID: 75149196011     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2009.00819.x     Document Type: Article

References (53)

1. Albon, S. D., A. Stien, R. J. Irvine, R. Langvatn, E. Ropstad, and O. Halvorsen. 2002. The role of parasites in the dynamics of a reindeer population. Proc. R. Soc. of Lond. B Biol. Sci. 269 : 1625 1632.
2. Anderson, R., and R. May. 1981. The population dynamics of microparasites and their invertebrate hosts. Philos. Trans. R. Soc. B Biol. Sci. 291 : 451 524.
3. Antonovics, J., and P. H. Thrall. 1994. The cost of resistance and the maintenance of genetic polymorphism in host-parasite systems. Proc. R. Soc. Lond. B Biol. Sci. 257 : 105 110.
4. Antonovics, J., D. Stratton, P. H. Thrall, and A. M. Jarosz. 1996. An anther-smut disease (Ustilago violacea) of fire-pink (Silene virginica: its Biology and Relationship to the anther-smut disease of white campion (Silene alba). Am. Midland Nat. 135 : 130 143.
5. Best, A., A. White, and M. Boots. 2008. The maintenance of host variation in tolerance to pathogens and parasites. Proc. Natl Acad. Sci. 105 : 20786 20791.
6. Best, A., A. White, and M. Boots. 2009. The implications of coevolutionary dynamics to host-parasite interactions. Am. Nat. 173 : 779 791.
7. Bonds, M. H. 2006. Host life-history strategy explains parasite-induced sterility. Am. Nat. 168 : 281 293.
8. Boots, M. 2004. Modelling insect diseases as functional predators. Physiol. Entemology 29 : 237 239.
9. Boots, M. 2008. Fight or learn to live with the consequences. Trends Ecol. Evol. 23 : 248 250.
10. Boots, M., and M. Begon. 1993. Trade-offs with resistance to a granulosis virus in the Indian meal moth, examined by a laboratory evolution experiment. Funct. Ecol. 7 : 528 534.
11. Boots, M., and R. G. Bowers. 1999. Three mechanisms of host resistance to microparasites - avoidance, recovery and tolerance - show different evolutionary dynamics. J. Theor. Biol. 201 : 13 23.
12. Boots, M., and R. G. Bowers. 2004. The evolution of resistance through costly acquired immunity. Proc. R. Soc. Lond. B Biol. Sci. 271 : 715 723.
13. Boots, M., and Y. Haraguchi. 1999. The evolution of costly resistance in host-parasite systems. Am. Nat. 153 : 359 370.
14. Boots, M., and M. Mealor. 2007. Local interactions select for lower pathogen infectivity. Science 315 : 1284 1286.
15. Boots, M., and R. Norman. 2000. Sublethal infection and the population dynamics of microparasite interactions. J. Anim. Ecol. 69 : 517 524.
16. Bowers, R. G., M. Boots, and M. Begon. 1994. Life-history trade-offs and the evolution of parasite resistance: competition between host strains. Proc. R. Soc. Lond. B Biol. Sci. 257 : 247 253.
17. Bowers, R. G., A. Hoyle, A. White, and M. Boots. 2005. The geometric theory of adaptive evolution: trade-off and invasion plots. J. Theor. Biol. 233 : 363 377.
18. Bremermann, H. J., and H. R. Thieme. 1989. A competitive exclusion principle for parasite virulence. J. Math. Biol. 27 : 179 190.
19. Brockerhoff, A. M. 2004. Occurrence of the internal parasite Portunion sp. (Isopoda: Entoniscidae) and its effect on reproduction in intertidal crabs (Decapoda: Grapsidae) from New Zealand. J. Parasitol. 90 : 1338 1344.
20. Caraco, T., S. Glavanakov, S. Li, W. Maniatty, and B. Szymanski. 2006. Spatially structured superinfection and the evolution of disease virulence. Theor. Popul. Biol. 69 : 367 384.
21. de Mazancourt, C., and U. Dieckmann. 2004. Trade-off geometries and frequency-dependent selection. Am. Nat. 164 : 765 778.
22. de Roode, J. C., R. Pansini, S. J. Cheesman, M. E. H. Helinski, S. Huijben, A. R. Wargo, A. S. Bell, B. H. K. Chan, and D. Walliker, A. F. Read. 2005. Virulence and competitive ability in genetically diverse malaria infections. Proc. Natl Acad. Sci. USA 102 : 7624 7628.
23. de Roode, J. C., A. J. Yates, and S. Altizer. 2008. Virulence- transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proc. Natl Acad. Sci. 105 : 7489 7494.
24. Deter, J., J. F. Cosson, Y. Chaval, N. Charbonnel, and S. Morand. 2007. The intestinal nematode Trichuris arvicolae affects the fecundity of its host, the common vole Microtus arvalis. Parasitol. Res. 101 : 1161 1164.
25. Dobson, A. P., and P. J. Hudson. 1992. Regulation and stability of a free-living host-parasite system: trichostrongylus tenius in red grouse. II. Population models. J. Anim. Ecol. 61 : 487 498.
26. Ebert, D., H. J. Carius, T. Little, and E. Decaestecker. 2004. The evolution of virulence when parasites cause host castration and gigantism. Am. Nat. 164 : S19 S32.
27. Feore, S. M., M. Bennett J. Chantrey, T. Jones, D. Baxby, and M. Begon. 1997. The effect of cowpox virus infection on fecundity in bank voles and wood mice. Proc. R. Soc. Lond. B Biol. Sci 264 : 1457 1461.
28. Frank, S. A. 1992. A kin selection model for the evolution of virulence. Proc. R. Soc. Lond. B Biol. Sci. 250 : 195 197.
29. Gandon, S., P. Agnew, and Y. Michalakis. 2002. Coevolution between parasite virulence and host life-history traits. Am. Nat. 160 : 374 388. (Pubitemid 34973772)
30. Geritz, S. A. H., E. Kisdi, G. Meszéna, and J. A. J. Metz. 1998. Evolutionarily singular strategies and the adaptive growth and branching of the evolutionary tree. Evol. Ecol. 12 : 35 57.
31. Godfray, H. C. J. 1993. Parasitoids: behavioral and evolutionary ecology. Princeton Univ. Press, Princeton.
32. Hoyle, A., R. G. Bowers, A. White, and M. Boots. 2008. The influence of trade-off shape on evolutionary behaviour in classical ecological scenarios. J. Theor. Biol. 250 : 498 511.
33. Hudson, P. J., D. Newborn, and A. P. Dobson. 1992. Regulation and stability of a free-living host-parasite system: trichostrongylus tenius in red grouse. I. Monitoring and parasite reduction experiments. J. Anim. Ecol. 61 : 477 486.
34. Jaenike, J. 1996. Suboptimal virulence of an insect-parasitic nematode. Evolution 50 : 2241 2247.
35. Kisdi, E. 2006. Trade-off geometries and the adaptive dynamics of two co-evolving species. Evol. Ecol. Res. 8 : 959 973.
36. Levin, S., and D. Pimentel. 1981. Selection of intermediate rates of increase in parasite-host systems. Am. Nat. 117 : 308 315.
37. Little, T. J., H. J. Carius, O. Sakwinska, and D. Ebert. 2002. Competitiveness and life-history characteristics of Daphnia with respect to susceptibility to a bacterial pathogen. J. Evol. Biol. 15 : 796 802.
38. Mackinnon, M. J., and A. F. Read. 1999. Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 53 : 689 703.
39. Marrow, P., Dieckmann, U., and Law, R. 1996. Evolutionary dynamics of predator-prey systems: an ecological perspective. J. Math. Biol. 24 : 556 578.
40. Metz, J. A. J., S. A. H. Geritz, G. Meszéna, F. J. A. Jacobs, and J. S. Van Heerwaarden. 1996. Adaptive dynamics: a geometrical study of the consequences of nearly faithful reproduction. Pp. 183 231 in S. J. van Strein and S. M. Verduyn Lunel, eds. Stochastic and Spatial Structures of Dynamical Systems. Elsevier, North-Holland.
41. Miller, M. R., A. White, and M. Boots. 2005. The evolution of parasites in response to tolerance in their hosts: the good, the bad and apparent commensalism. Evolution 60 : 945 956.
42. Miller, M. R., A. White, and M. Boots. 2006. The evolution of host resistance: tolerance and control as distinct strategies. J. Theor. Biol. 236 : 198 207.
43. Miller, M. R., A. White, and M. Boots. 2007. Host life span and the evolution of resistance characteristics. Evolution 61 : 2 14.
44. Nowak, M. A., and R. M. May. 1994. Superinfection and the evolution of parasite virulence. Proc. R. Soc. Lond. B Biol. Sci. 255 : 81 89.
45. O'Keefe, K. J., and J. Antonovics. 2002. Playing by different rules: the evolution of virulence in sterlizing parasites. Am. Nat. 159 : 597 605.
46. Råberg, L., D. Sim, and A. F. Read. 2007. Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318 : 812 814.
47. Restif, O., and J. C. Koella. 2004. Concurrent evolution of resistance and tolerance to pathogens. Am. Nat. 164 : E90 E102.
48. Roy, B. A., and J. W. Kirchner. 2000. Evolutionary dynamics of parasite resistance and tolerance. Evolution 54 : 51 63.
49. Simms, E. L., and J. Triplett. 1994. Costs and benefits of plant responses to disease: resistance and tolerance. Evolution 48 : 1973 1985.
50. Smith, M., A. White, J. A. Sherratt, S. Telfer, M. Begon, and X. Lambin. 2008. Disease effects on reproduction can cause population cycles in seasonal environments. J. Anim. Ecol. 77 : 378 389.
51. Svennnungsen, T., and Kisdi, E. 2009. Evolutionary branching of virulence in a single-infection model. J. Theor. Biol. 257 : 408 418.
52. Tiffin, P., and M. D. Rausher. 1999. Genetic constraints and selection acting on tolerance to herbivory in the common morning glory Ipomoea purpurea. Am. Nat. 154 : 700 716.
53. Wickham, M. E., N. F. Brown, E. C. Boyle, B. K. Coombes, and B. B. Finlay. 2007. Virulence is positively selected by transmission success between mammalian hosts. Curr. Biol. 17 : 783 788.