A unified model for the coevolution of resistance, tolerance, and virulence

Evolution

Volumn 64, Issue 10, 2010, Pages 2988-3009

  Carval, Dominique ^a   Ferriere, Regis ^b,c  

^a UPMC University Paris 06   (France)

^b ECOLE NORMALE SUPÉRIEURE   (France)

^c University of Arizona   (United States)

Author keywords

Adaptive dynamics; Host defense; Infection; Parasitism; Pathogen; Trade offs

Indexed keywords

COEVOLUTION; DEFENSE BEHAVIOR; EPIDEMIOLOGY; INFECTIVITY; MODEL TEST; MORTALITY; PARASITE RESISTANCE; PARASITISM; PATHOGEN; TOLERANCE; TRADE-OFF; VIRULENCE;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; DRUG TOLERANCE; EVOLUTION; GENETICS; HOST PARASITE INTERACTION; IMMUNOLOGICAL TOLERANCE; PARASITE; PHYSIOLOGY; POPULATION DYNAMICS; VIRULENCE;

ANIMALS; BIOLOGICAL EVOLUTION; DRUG TOLERANCE; HOST-PARASITE INTERACTIONS; IMMUNE TOLERANCE; MODELS, BIOLOGICAL; PARASITES; POPULATION DYNAMICS; VIRULENCE;

EID: 78649288091     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2010.01035.x     Document Type: Article

References (84)

1. Alizon, S., and M. van Baalen. 2005. Emergence of a convex trade-off between transmission and virulence. Am. Nat. 165:E155-E167.
2. Alizon, S., and M. van Baalen. 2008. Multiple infections, immune dynamics, and the evolution of virulence. Am. Nat. 172:E150-E168.
3. Alizon, S., A. Hurford, N. Mideo, and M. van Baalen. 2009. Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J. Evol. Biol. 22:245-259.
4. Anderson, R. M., and R. M. May. 1979. Population biology of infectious diseases: part I. Nature 280:361-367.
5. Anderson, R. M., and R. M. May. 1982. Coevolution of hosts and parasites. Parasitology 85:411-426.
6. André, J. B., and S. Gandon. 2006. Vaccination, within-host dynamics, and virulence evolution. Evolution 60:13-23.
7. André, J. B., J. B. Ferdy, and B. Godelle. 2003. Within-host parasite dynamics, emerging trade-off, and the evolution of virulence with immune system. Evolution 57:1489-1497.
8. Antonovics, J., and P. H. Thrall. 1994. The cost of resistance and the maintenance of genetic polymorphism in host-pathogen systems. Proc. R. Soc. Lond. B 247:105-110.
9. Athreya, K. B. 1993. Rates of decay for the survival probability of a mutant gene. II. The multitype case. J. Math. Biol. 32:45-53.
10. Athreya, K. B., and P. E. Ney. 1972. Branching processes. Springer-Verlag, New York.
11. Ayres, J. S., and D. S. Schneider. 2008. A signaling protease required for melanization in Drosophila affects resistance and tolerance of infections. PLoS Biol. 6:2764-2773.
12. Barker, K. R. 1993. Resistance/tolerance and related concepts/terminology in plant nematology. Plant Disease 77:111-113.
13. Baucom, R. S., and R. Mauricio. 2008. Constraints on the evolution of tolerance to herbicide in the common morning glory: resistance and tolerance are mutually exclusive. Evolution 62:2842-2854.
14. Best, A., A. White, and M. Boots. 2009. The implications of coevolutionary dynamics to host-parasite interactions. Am. Nat. 173:779-791.
15. Bonds, M. H. 2006. Host life-history strategy explains pathogen-induced sterility. Am. Nat. 168:281-293.
16. Bonhoeffer, S., R. E. Lenski, and D. Ebert. 1996. The curse of the pharaoh: the evolution of virulence in pathogens with long living propagules. Proc. R. Soc. London B. 263:715-721.
17. Boots, M. 2008. Fight or learn to live with the consequences? Trends Ecol. Evol. 23:248-250.
18. Boots, M., and M. Begon. 1993. Trade-off with resistance to a granulosis virus in the Indian meal moth, examined by a laboratory evolution experiment. Funct. Ecol. 7:528-534.
19. Bowers, R. G., M. Boots, and M. Begon. 1994. Life-history trade-offs and the evolution of pathogen resistance: competition between host strains. Proc. R. Soc. Lond. B 257:247-253.
20. Carr, D. E., J. F. Murphy, and M. D. Eubanks. 2006. Genetic variation and covariation for resistance and tolerance to Cucumber mosaic virus in Mimulus guttatus Phrymaceae: a test for costs and constraints. Heredity 96:29-38.
21. Champagnat, N., R. Ferriere, and S. Meleard. 2006. Unifying evolutionary dynamics: from individual stochastic processes to macroscopic models. Theor. Popul. Biol. 69:297-321.
22. Clarke, D. D. 1986. Tolerance of parasites and disease in plants and its significance in host-parasite interactions. Adv. Plant Pathol. 5:161-197.
23. Day, T. 2001. Parasite transmission modes and the evolution of virulence. Evolution 55:2389-2400.
24. Day, T. 2002. Virulence evolution via host exploitation and toxin production in spore-producing pathogens. Ecol. Lett. 5:471-476.
25. Day, T., and S. Gandon. 2007. Applying population-genetic models in theoretical evolutionary epidemiology. Ecol. Lett. 10:876-888.
26. Dercole, F., J. O. Irisson, and S. Rinaldi. 2006a. Bifurcation analysis of a predator-prey coevolution model. SIAM J. Appl. Math. 63:1378-1391.
27. Dercole, F., R. Ferriere, A. Gragnani, and S. Rinaldi. 2006b. Coevolution of slow-fast populations: evolutionary sliding, evolutionary pseudo- equilibria and complex Red Queen dynamics. Proc. Biol. Sci. 273:983-990.
28. Dercole, F., and S. Rinaldi. 2008. Analysis of evolutionary processes. Princeton Univ. Press, Princeton, NJ.
29. Dieckmann, U., and R. Law. 1996. The dynamical theory of coevolution: a derivation from stochastic ecological processes. J. Math. Biol. 34:579-612.
30. Dieckmann, U., J. A. J. Metz, M. W. Sabelis, and K. Sigmund. 2002. Adaptative dynamics of infectious diseases. Cambridge Univ. Press, Cambridge.
31. Ebert, D., and J. J. Bull. 2003. Challenging the trade-off model for the evolution of virulence: is virulence management feasible? Trends Microbiol. 11:15-20.
32. Ebert, D., and W. W. Weisser. 1997. Optimal killing for obligate killers: the evolution of life histories and virulence of semelparous parasites. Proc. Biol. Sci. 264:985-991.
33. Ewald, P. W. 1993. Evolution of virulence. Sci. Am. 268:86-93.
34. Ewald, P. W. 1994. The evolution of infectious diseases. Oxford Univ. Press, Oxford.
35. Fineblum, W. L., and M. D. Rausher. 1995. Trade-off between resistance and tolerance to herbivore damage in a morning glory. Nature 377:517-520.
36. Fornoni, J., P. L. Valverde, and J. Nunez-Farfan. 2003. Quantitative genetics of plant tolerance and resistance against natural enemies of two natural populations of Datura stramonium. Evol. Ecol. Res. 5:1049-1065.
37. Fornoni, J., J. Nunez-Farfan, P. L. Valverde, and M. D. Rausher. 2004. Evolution of mixed plant defense allocation against natural enemies. Evolution 58:1685-1695.
38. Frank, S. A. 1996. Models of parasite virulence. Q. Rev. Biol. 71:37-78.
39. Gandon, S., V. A. Jansen, and M. van Baalen. 2001. Host life history and the evolution of parasite virulence. Evolution 55:1056-1062.
40. Gandon, S., M. van Baalen, and V. A. Jansen. 2002. The evolution of parasite virulence, superinfection, and host resistance. Am. Nat. 159:658-669.
41. Gilchrist, M. A., and A. Sasaki. 2002. Modeling host-parasite coevolution: a nested approach based on mechanistic models. J. Theor. Biol. 218:289-308.
42. Gilchrist, M. A., D. Coombs, and A. S. Perelson. 2004. Optimizing within- host viral fitness: infected cell lifespan and virion production rate. J. Theor. Biol. 229:281-288.
43. Hochberg, M. E., and M. van Baalen. 1998. Antagonistic coevolution over productivity gradients. Am. Nat. 152:620-634.
44. Hochberg, M. E., R. Gomulkiewicz, R. D. Holt, and J. N. Thompson. 2000. Weak sinks could cradle mutualistic symbioses: strong sources should harbour parasitic symbioses. J. Evol. Biol. 13:213-222.
45. Hofbauer, J., and K. Sigmund. 1998. Evolutionary games and population dynamics. Cambridge Univ. Press, Cambridge.
46. Khibnik, A. I., and A. S. Kondrashov. 1997. Three mechanisms of Red Queen dynamics. Proc. R. Soc. Lond. B 264:1049-1056.
47. Kisdi, E. 1999. Evolutionary branching under asymmetric competition. J. Theor. Biol. 197:149-162.
48. Koella, J., and C. Boete. 2003. A model for the coevolution of immunity and immune evasion in vector-borne diseases with implications for the epidemiology of malaria. Am. Nat. 161:698-707.
49. Kostitzin, V. A. 1934. Symbiose, parasitisme et évolution (étude mathématique). Actualités Scientifiques et Industrielles 96:337-381.
50. Kover, P. X., and B. A. Schaal. 2002. Genetic variation for disease resistance and tolerance among Arabidopsis thaliana accessions. Proc. Natl. Acad. Sci. USA 99:11270-11274.
51. Law, R., and U. Dieckmann. 1998. Symbiosis through exploitation and the merger of lineages in evolution. Proc. R. Soc. Lond. B. 265:1245-1253.
52. Le Galliard, J. F., R. Ferriere, and U. Dieckmann. 2005. Adaptive evolution of social traits: origin, trajectories, and correlations of altruism and mobility. Am. Nat. 165:206-224.
53. Lenski, R. E., and R. M. May. 1994. The evolution of virulence in parasites and pathogens: reconciliation between two competing hypotheses. J. Theor. Biol. 169:253-265.
54. Mauricio, R., M. D. Rausher, and D. S. Burdick. 1997. Variation in the defense strategies of plants: are resistance and tolerance mutually exclusive? Ecology 78:1301-1310.
55. Metz, J. A. J., R. M. Nisbet, and S. A. H. Geritz. 1992. How should we define 'fitness' for general ecological scenarios? Trends. Ecol. Evol. 7:198-202.
56. Metz, J. A. J., S. A. H. Geritz, G. Meszena, 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 Strien and S. M. Verduyn Lunel, eds. Stochastic and spatial structures of dynamical systems. North Holland, Amsterdam.
57. Mideo, N., S. Alizon, and T. Day. 2008. Linking within- and between-hot dynamics in the evolutionary epidemiology of infectious diseases. Trends. Ecol. Evol. 23:511-517.
58. Miller, M. R., A. White, and M. Boots. 2005. The evolution of host resistance: tolerance and control as distinct strategies. J. Theor. Biol. 236:198-207.
59. Miller, M. R., A. White, and M. Boots. 2006. The evolution of parasites in response to tolerance in their hosts: the good, the bad, and apparent commensalism. Evolution 60:945-956.
60. Nowak, M. A., and K. Sigmund. 1992. Tif-For-Tat in heterogeneous populations. Nature 355:250-253.
61. Pugliese, A. 2002. On the evolutionary coexistence of parasite strains. Math Biosci. 177:355-375.
62. Raberg, L., D. Sim, and A. F. Read. 2007. Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318:812-814.
63. Raberg, L., A. L. Graham, and A. F. Read. 2009. Decomposing health: tolerance and resistance to parasites and animals. Philos. Trans. R. Soc. Biol. Sci. 364:37-49.
64. Rausher, M. D. 2001. Co-evolution and plant resistance to natural enemies. Nature 411:857-864.
65. Restif, O., and J. C. Koella. 2003. Shared control of epidemiological traits in a coevolutionary model of host-parasite interactions. Am. Nat. 161:827-836.
66. Restif, O., and J. C. Koella. 2004. Concurrent evolution of resistance and tolerance to pathogens. Am. Nat. 164:E90-E102.
67. Roy, B. A., and J. W. Kirchner. 2000. Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54:51-63.
68. Rueffler, C., M. Egas, and J. A. J. Metz. 2006. Evolutionary predictions should be based on individual-level traits. Am. Nat. 168:E148-E162.
69. Sasaki, A. 2000. Host-parasite coevolution in a multilocus gene-for-gene system. Proc. Biol. Sci. 267:2183-2188.
70. Schmid-Hempel, P., and S. A. Frank. 2007. Pathogenesis, virulence, and infective dose. PLoS Pathog. 3:1372-1373.
71. Simms, E. L., and J. Triplett. 1994. Costs and benefits of plant responses to disease: resistance and tolerance. Evolution 48:1973-1985.
72. Stowe, K. A. 1998. Experimental evolution of resistance in Brassica rapa: correlated response in lines selected for glucosinolate content. Evolution 52:703-712.
73. Svennungsen, T. O., and E. Kisdi. 2009. Evolutionary branching of virulence in a single-infection model. J. Theor. Biol. 257:408-418.
74. Thompson, J. N. 1994. The coevolution process. Univ. of Chicago Press, Chicago.
75. Tiffin, P. 2000. Are tolerance, avoidance, and antibiosis evolutionarily and ecologically equivalent responses of plants to herbivores? Am. Nat. 155:128-138.
76. 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.
77. van Baalen, M. 1998. Coevolution of recovery ability and virulence. Proc. R. Soc. Lond. B 265:317-325.
78. van Baalen, M., and V. A. A. Jansen. 2001. Dangerous liaisons: the ecology of private interest and common good. Oikos 95:211-224.
79. van Baalen, M., and M. W. Sabelis. 1995. The dynamics of multiple infection and the evolution of virulence. Am. Nat. 146:881-910.
80. Vanderplank, J. E., Ed. 1984. Disease resistance in plants. Academic Press, Orlando.
81. Vera Cruz, C. M., J. F. Bai, I. Ona, H. Leung, R. J. Nelson, T. W. Mew, and J. E. Leach. 2000. Predicting durability of a disease resistance gene based on an assessment of the fitness loss and epidemiological consequences of avirulence gene mutation. Proc. Natl. Acad. Sci. USA 97:13500-13505.
82. Weinig, C., L. A. Dorn, N. C. Kane, Z. M. German, S. S. Halldorsdottir, M. C. Ungerer, Y. Toyonaga, T. F. C. Mackay, M. D. Purugganan, and J. Schmitt. 2003. Heterogeneous selection at specific loci in natural environments in Arabidopsis thaliana. Genetics 165:321-329.
83. Wolin, C. 1985. The population dynamics of mutualistic systems. Pp. 248-269 in D. H. Boucher, ed. The biology of mutualism. Oxford University Press, New York.
84. Woolhouse, M. E. J., J. P. Webster, E. Domingo, B. Charlesworth, and B. R. Levin. 2002. Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat. Genet. 32:569-577.