Virulence evolution and the trade-off hypothesis: History, current state of affairs and the future

Journal of Evolutionary Biology

Volumn 22, Issue 2, 2009, Pages 245-259

  Alizon, S ^a,b   Hurford, A ^a   Mideo, N ^a   Van Baalen, M ^c  

^a QUEEN S UNIVERSITY   (Canada)

^b ETH ZURICH   (Switzerland)

^c ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

Evolution; Immune response; Infectious diseases; Multiple infections; Recovery; Trade off; Transmission; Virulence

Indexed keywords

ADAPTATION; ECOLOGICAL MODELING; EVOLUTIONARY BIOLOGY; IMMUNE RESPONSE; IMMUNE SYSTEM; INFECTIOUS DISEASE; LIFE HISTORY TRAIT; PARASITE TRANSMISSION; TRADE-OFF; VIRULENCE;

ANIMAL; EVOLUTION; PARASITE; PARASITOLOGY; PATHOGENICITY; REVIEW; VIRULENCE;

ANIMALS; EVOLUTION; PARASITES; PARASITOLOGY; VIRULENCE;

EID: 58549116149     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2008.01658.x     Document Type: Review

References (123)

1. Agnew, P. Koella, J.C. 1997. Virulence, parasite mode of transmission, and host fluctuating asymmetry. Proc. R. Soc. Lond. B 264 : 9 15. doi :.
2. Alizon, S. 2008a. Dcreased overall virulence in co-infected hosts leads to the persistence of virulent parasites. Am. Nat. 172 : E67 E79. doi :.
3. Alizon, S. 2008b. Transmission-recovery trade-offs to study parasite evolution. Am. Nat. 172 : E113 E121 doi :.
4. Alizon, S. van Baalen, M. 2005. Emergence of a convex trade-off between transmission and virulence. Am. Nat. 165 : E155 E167 doi :.
5. Alizon, S. van Baalen, M. 2008a. The emergence of transmission-virulence trade-offs in vector-borne diseases. Theor. Popul. Biol. 74 : 6 15. doi :.
6. Alizon, S. van Baalen, M. 2008b. Multiple infections, immune dynamics and virulence evolution. Am. Nat. 172 : 150 158. doi :.
7. Anderson, R.M. May, R.M. 1979. Population biology of infectious diseases. Nature 280 : 361 367. doi :.
8. Anderson, R.M. May, R.M. 1982. Coevolution of hosts and parasites. Parasitology 85 : 411 426.
9. André, J.B. van Baalen, M. 2007. Collective traits in pathogenic bacteria. In : Evolutionary Biology of Bacterial and Fungal Pathogens (F. Baquero, C. Nombela, G.H. Cassell J.A. Gutiérrez, eds pp. 13 20. ASM Press, New York.
10. André, J.B., Ferdy, J.B. Godelle, B. 2003. Within-host parasite dynamics, emerging trade-off, and evolution of virulence with immune system. Evolution 57 : 1489 1497. doi :.
11. van Baalen, M. 2002. Contact networks and the evolution of virulence - implications for virulence management. In : The Adaptive Dynamics of Infectious Diseases: In Pursuit of Virulence Management (U. Dieckmann, J.A.J. Metz, M.W. Sabelis K. Sigmund, eds pp. 85 103. Cambridge University Press, Cambridge.
12. van Baalen, M. Sabelis, M.W. 1995. The dynamics of multiple infection and the evolution of virulence. Am. Nat. 146 : 881 910. doi :.
13. Ball, G.H. 1943. Parasitism and evolution. Am. Nat. 77 : 345 364. doi :.
14. van Ballegooijen, W.M. Boerlijst, M.C. 2004. Emergent trade-offs and selection for outbreak frequency in spatial epidemics. Proc. Natl. Acad. Sci. USA 101 : 18246 18250. doi :.
15. Bedhomme, S., Agnew, P., Vital, Y., Sidobre, C. Michalakis, Y. 2005. Prevalence-dependent costs of parasite virulence. PLoS. Biol. 3 : 262 doi :.
16. Bell, A.S., de Roode, J.C., Sim, D. Read, A.F. 2006. Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution 60 : 1358 1371. doi :.
17. van Beneden, P.J. 1875. Les commensaux et les parasites dans le règne animal. G. Baillière, Paris.
18. Bonds, M.H. 2006. Host life-history strategy explains pathogen-induced sterility. Am. Nat. 168 : 281 293. doi :.
19. Boots, M. Mealor, M. 2007. Local interactions select for lower pathogen infectivity. Science 315 : 1284 1286. doi :.
20. Bremermann, H.J. Pickering, J. 1983. A game-theoretical model of parasite virulence. J. Theor. Biol. 100 : 411 426. doi :.
21. Brown, S.P., Hochberg, M.E. Grenfell, B.T. 2002. A game-theoretical model of parasite virulence. J. Theor. Biol. 10 : 401 405. doi :.
22. Brown, N.F., Wickham, M.E., Coombes, B.K. Finlay, B.B. 2006. Crossing the line: selection and evolution of virulence traits. PLoS Pathol. 2 : e42 doi :.
23. Buckling, A. Brockhurst, M.A. 2008. Kin selection and the evolution of virulence. Heredity 100 : 484 488. doi :.
24. Bull, J.J. 1994. Virulence. Evolution 48 : 1423 1437.
25. Casadevall, A. Pirofski, L.A. 1999. Host-pathogen interactions: redefining the basic concepts of virulence and pathogenicity. Infect. Immun. 67 : 3703 3713.
26. Coombs, D., Gilchrist, M.A. Ball, C.L. 2007. Evaluating the importance of within-and between-host selection pressures on the evolution of chronic pathogens. Theor. Popul. Biol. 72 : 576 591. doi :.
27. Cooper, V.S., Reiskind, M.H., Miller, J.A., Shelton, K.A., Walther, B.A., Elkinton, J.S. Ewald, P.W. 2002. Timing of transmission and the evolution of virulence of an insect virus. Proc. R. Soc. Lond. B 269 : 1161 1165. doi :.
28. Day, T. 2001. Parasite transmission modes and the evolution of virulence. Evolution 55 : 2389 2400. doi :.
29. Day, T. 2002. On the evolution of virulence and the relationship between various measures of mortality. Proc. R. Soc. Lond. B 269 : 1317 1323. doi :.
30. Day, T. 2003. Virulence evolution and the timing of disease life-history events. Trends Ecol. Evol. 18 : 113 118. doi :.
31. Day, T. Gandon, S. 2006. Insights from Price's equation into evolutionary epidemiology. In : Disease Evolution: Models, Concepts, and Data Analyses (Z. Feng, U. Dieckmann S.A. Levin, eds). pp. 23 44. DIMACS Series in Discrete Mathematics and Theoretical Computer Science; 71. American Mathematical Society.
32. Day, T. Gandon, S. 2007. Applying population-genetic models in theoretical evolutionary epidemiology. Ecol. Lett. 10 : 876 888. doi :.
33. Day, T. Proulx, S.R. 2004. A general theory for the evolutionary dynamics of virulence. Am. Nat. 163 : E40 E63. doi :.
34. Day, T., Graham, A. Read, A. 2007. Evolution of parasite virulence when host responses cause disease. Proc. R. Soc. Lond. B 274 : 2685 2692. doi :.
35. Day, T., Mideo, N. Alizon, S. 2008. Why is HIV not vector-borne Evol. Appl. 1 : 17 27. doi :.
36. Dieckmann, U., Metz, J.A.J., Sabelis, M.W. Sigmund, K. (eds) 2002. Adaptive Dynamics of Infectious Diseases. In Pursuit of Virulence Management. Cambridge Studies in Adaptive Dynamics. Cambridge University Press, Cambridge.
37. Diekmann, O. Heesterbeek, J. 2000. Mathematical Epidemiology of Infectious Diseases: Model Building, Analysis, and Interpretation. Wiley, New York.
38. Donoghue, H.D., Spigelman, M., Greenblatt, C.L., Lev-Maor, G., Bar-Gal, G.K., Matheson, C., Vernon, K., Nerlich, A.G. Zink, A.R. 2004. Tuberculosis: from prehistory to robert koch, as revealed by ancient DNA. Lancet Infect. Dis. 4 : 584 592. doi :.
39. Dwyer, G., Levin, S.A. Buttel, L. 1990. A simulation model of the population dynamics and evolution of myxomatosis. Ecol. Monogr. 60 : 423 447.
40. Ebert, D. 1998. Experimental evolution of parasites. Science 282 : 1432 1435. doi :.
41. Ebert, D. 1999. The evolution and expression of parasite virulence. In : Evolution in Health and Disease (S.C. Stearns, ed. pp. 161 172. University Press, Oxford.
42. Ebert, D. Bull, J.J. 2003. Challenging the trade-off model for the evolution of virulence: is virulence management feasible? Trends Microbiol. 11 : 15 20. doi :.
43. Ebert, D. Bull, J.J. 2008. The evolution and expression of virulence. In : Evolution in Health and Disease (S. Stearns J. Koella, eds. pp. 153 167. Oxford University Press, Oxford, USA.
44. Ebert, D. Herre, E.A. 1996. The evolution of parasitic diseases. Parasitol. Today 12 : 96 101. doi :.
45. Ewald, P.W. 1983. Host-parasite relations, vectors, and the evolution of disease severity. Annu. Rev. Ecol. Evol. Syst. 14 : 465 485. doi :.
46. Ewald, P.W. 1994. Evolution of Infectious Disease. Oxford University Press, Oxford.
47. Fenner, F. Ratcliffe, F. 1965. Myxomatosis. Cambridge University Press.
48. Ferguson, H.M., Mackinnon, M.J., Chan, B.H. Read, A.F. 2003. Mosquito mortality and the evolution of malaria virulence. Evolution 57 : 2792 2804. doi :.
49. Frank, S.A. 1996. Models of parasite virulence. Q. Rev. Biol. 71 : 37 78. doi :.
50. Frank, S.A. Schmid-Hempel, P. 2008. Mechanisms of pathogenesis and the evolution of parasite virulence. J. Evol. Biol. 21 : 396 404. doi :.
51. Fraser, C., Hollingsworth, T.D., Chapman, R., de Wolf, F. Hanage, W.P. 2007. Variation in HIV-1 set-point viral load: epidemiological analysis and an evolutionary hypothesis. Proc. Natl. Acad. Sci. USA 104 : 17441 17446. doi :.
52. Gandon, S. 2004. Evolution of multihost parasites. Evolution 58 : 455 469. doi :.
53. Gandon, S. Day, T. 2003. Understanding and managing pathogen evolution: a way forward. Trends Microbiol. 11 : 206 207. doi :.
54. Gandon, S. Michalakis, Y. 2000. Evolution of parasite virulence against qualitative or quantitative host resistance. Proc. R. Soc. Lond. B 267 : 985 990. doi :.
55. Gandon, S., Mackinnon, M.J., Nee, S. Read, A.F. 2001. Imperfect vaccines and the evolution of pathogen virulence. Nature 414 : 751 756. doi :.
56. Gandon, S., Mackinnon, M.J., Nee, S. Read, A.F. 2002a. Antitoxin vaccines and pathogen virulence (reply). Nature 417 : 610.
57. Gandon, S., van Baalen, M. Jansen, V.A.A. 2002b. The evolution of parasite virulence, superinfection and host resistance. Am. Nat. 159 : 658 669. doi :.
58. Gandon, S., Mackinnon, M.J., Nee, S. Read, A.F. 2003. Imperfect vaccination: some epidemiological and evolutionary consequences. Proc. R. Soc. Lond. B 270 : 1129 1136. doi :.
59. Ganusov, V.V., Bergstrom, C.T. Antia, R. 2002. Within-host population dynamics and the evolution of microparasites in a heterogeneous host population. Evolution 52 : 213 223. doi :.
60. Geritz, S.A.H., Metz, J.A.J., Kisdi, E. Meszéna, G. 1997. Dynamics of adaptation and evolutionary branching. Phys. Rev. Lett. 78 : 2024 2027. doi :.
61. Gilchrist, M.A. Sasaki, A. 2002. Modeling host-parasite coevolution: a nested approach based on mechanistic models. J. Theor. Biol. 218 : 289 308. doi :.
62. Gilchrist, M.A., Coombs, D. Perelson, A.S. 2004. Optimizing within-host viral fitness: infected cell lifespan and virion production rate. J. Theor. Biol. 229 : 281 288. doi :.
63. Graham, A.L., Allen, J.E. Read, A.F. 2005. Evolutionary causes and consequences of immunopathology. Annu. Rev. Ecol. Evol. Syst. 36 : 373 397. doi :.
64. Grech, K., Watt, K. Read, A.F. 2006. Host-parasite interactions for virulence and resistance in a malaria model system. J. Evol. Biol. 19 : 1620 1630. doi :.
65. Grenfell, B. Harwood, J. 1997. (Meta)population dynamics of infectious diseases. Trends Ecol. Evol. 12 : 395 399. doi :.
66. Griffin, A.S., West, S.A. Buckling, A. 2004. Cooperation and competition in pathogenic bacteria. Nature 430 : 1024 1027. doi :.
67. Hamilton, W. 1964. The genetical evolution of social behaviour (I & II). J. Theor. Biol. 7 : 1 52. doi :.
68. Haraguchi, Y. Sasaki, A. 2000. The evolution of parasite virulence and transmission rate in a spatially structured population. J. Theor. Biol. 203 : 85 96. doi :.
69. Harrison, F., Browning, L.E., Vos, M. Buckling, A. 2006. Cooperation and virulence in acute Pseudomonas aeruginosa infections. BMC Biol. 4 : 21 5. doi :.
70. Herre, E.A. 1993. Population structure and the evolution of virulence in nematode parasites of fig wasps. Science 259 : 1442 1445. doi :.
71. Horak, P., Saks, L., Karu, U. Ots, I. 2006. Host resistance and parasite virulence in greenfinch coccidiosis. J. Evol. Biol. 19 : 277 288. doi :.
72. Jensen, K.H., Little, T., Skorping, A. Ebert, D.V. 2006. Empirical support for optimal virulence in a castrating parasite. PLoS. Biol. 4 : e197 doi
73. Kamo, M., Sasaki, A. Boots, M. 2007. The role of trade-off shapes in the evolution of parasites in spatial host populations: an approximate analytical approach. J. Theor. Biol. 244 : 588 596. doi :.
74. Kostitzin, V.A. 1934. Symbiose, Parasitisme et Évolution, actualités scientifiques et culturelles edn. Hermann, Paris.
75. Levin, B.R. Bull, J.J. 1994. Short-sighted evolution and the virulence of pathogenic microorganisms. Trends Microbiol. 2 : 76 81. doi :.
76. Levin, S. Pimentel, D. 1981. Selection of intermediate rates of increase in parasite-host systems. Am. Nat. 117 : 308 315. doi :.
77. Lipsitch, M. Moxon, E.R. 1997. Virulence and transmissibility of pathogens: what is the relationship?. Trends Microbiol. 5 : 31 37. doi
78. Little, T.J., Chadwick, W. Watt, K. 2008. Parasite variation and the evolution of virulence in a Daphnia-microparasite system. Parasitology 135 : 303 308. doi :.
79. Lively, C.M. 2006. The ecology of virulence. Ecol. Lett. 9 : 1089 1095. doi :.
80. Long, G.H., Chan, B.H.K., Allen, J.E., Read, A.F. Graham, A.L. 2008. Experimental manipulation of immune-mediated disease and its fitness costs for rodent malaria parasites. BMC Evol. Biol. 8 : 128. doi :.
81. Mackinnon, M.J. Read, A.F. 1999a. Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 53 : 689 703.
82. Mackinnon, M.J. Read, A.F. 1999b. Selection for high and low virulence in the malaria parasite Plasmodium chabaudi. Proc. R. Soc. Lond. B 266 : 741 748. doi :.
83. Mackinnon, M.J. Read, A.F. 2003. The effect of host immunity on virulence-transmissibility relationships in the rodent malaria parasite Plasmodium chabaudi. Parasitology 126 : 103 112. doi
84. Mackinnon, M.J. Read, A.F. 2004. Virulence in malaria: an evolutionary viewpoint. Philos. Trans. R. Soc. B 359 : 965 986. doi :.
85. Mackinnon, M.J., Gaffney, D.J. Read, A.F. 2002. Virulence of malaria parasites: host genotype by parasite genotype interactions. Infect. Genet. Evol. 1 : 287 293. doi :.
86. Mackinnon, M.J., Gandon, S. Read, A.F. 2008. Virulence evolution in response to vaccination: the case of malaria. Vaccine 26S : C42 C52. doi :.
87. Manchester, K. 1984. Tuberculosis and leprosy in antiquity: an interpretation. Med. Hist. 28 : 162 173.
88. Massad, E. 1987. Transmission rates and the evolution of pathogenicity. Evolution 41 : 1127 1130.
89. Massey, R.C., Buckling, A. ffrench Constant, R. 2004. Interference competition and parasite virulence. Proc. R. Soc. Lond. B 271 : 785 788. doi :.
90. May, R.M. Anderson, R.M. 1983. Epidemiology and genetics in the coevolution of parasites and hosts. Proc. R. Soc. Lond. B 219 : 281 313. doi :.
91. Maynard Smith, J. 1982. Evolution and the Theory of Games. Cambridge University Press, Cambridge.
92. McKendrick, A.G. 1926. Applications of mathematics to medical problems. Proc. Edinburgh Math. Soc. 44 : 98 130.
93. Mendelsohn, J.A. 2002. 24:3-36. 'like all that lives' : biology, medicine and bacteria in the age of Pasteur and Koch. Hist. Philos. Life. Sci. 24 : 3-36. Day, T. 2008. Linking within- and between-host dynamics in the evolutionary epidemiology of infectious diseases. Trends Ecol. Evol. 23 : 511 517. doi :.
94. Miller, M.R., White, A. Boots, M. 2007. Host life span and the evolution of resistance characteristics. Evolution 61 : 2 14. doi :.
95. Miura, K., Keister, D.B., Muratova, O.V., Sattabongkot, J., Long, C.A. Saul, A. 2007. Transmission-blocking activity induced by malaria vaccine candidates Pfs25/Pvs25 is a direct and predictable function of antibody titer. Malar J6 : 107 doi :.
96. Molineaux, L. Dietz, K. 1999. Review of intra-host models of malaria. Parassitologia 41 : 221 231.
97. Nowak, M.A. May, R.M. 1994. Superinfection and the evolution of parasite virulence. Proc. R. Soc. Lond. B 255 : 81 89. doi :.
98. O'Keefe, J. K. Antonovics, J. 2002. Playing by different rules: the evolution of virulence in sterilizing pathogens. Am. Nat. 159 : 597 605. doi :.
99. Pasteur, L., Chamberlain, C.E. Roux, E. 1881. Compte rendu sommaire des expériences faites à Pouilly-le-Fort, près Melun, sur la vaccination charbonneuse. Comptes-rendus des séances de l'Académie des Sciences 92 : 1378 1383.
100. Paul, R.E.L., Lafond, T., Müller-Graf, C.D.M., Nithiuthai, S., Brey, P.T. Koella, J.C. 2004. Experimental evaluation of the relationship between lethal or non-lethal virulence and transmission success in malaria parasite infections. BMC Evol. Biol. 4 : 30. doi :.
101. Poulin, R. Combes, C. 1999. The concept of virulence: interpretations and implications. Parasitol. Today 15 : 474 475. doi :.
102. Price, P.W., Westoby, M., Rice, B., Atsatt, P.R., Fritz, R.S., Thompson, J.N. Mobley, K. 1986. Parasite mediation in ecological interactions. Annu. Rev. Ecol. Syst. 17 : 487 505. doi :.
103. Raberg, L., Sim, D. Read, A.F. 2007. Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318 : 812 814. doi :.
104. Rand, D.A., Keeling, M. Wilson, H.B. 1995. Invasion, stability and evolution to criticality in spatially extended, artificial host-pathogen ecologies. Proc. R. Soc. Lond. B 259 : 55 63. doi :.
105. Read, A. 1994. The evolution of virulence. Trends Microbiol. 2 : 73 76. doi :.
106. Read, J.M. Keeling, M.J. 2006. Disease evolution across a range of spatio-temporal scales. Theor. Popul. Biol. 70 : 201 213. doi :.
107. Read, A.F. Taylor, L.H. 2001. The ecology of genetically diverse infections. Science 292 : 1099 1102. doi :.
108. de Roode, J.C., Pansini, R., Cheesman, S.J., Helinski, M.E.H., Huijben, S., Wargo, A.R., Bell, A.S., Chan, B.H.K., Walliker, D. Read, A.F. 2005. Virulence and competitive ability in genetically diverse malaria infections. Proc. Natl. Acad. Sci. USA 102 : 7624 7628. doi :.
109. de Roode, J.C., Yates, A.J. Altizer, S. 2008. Virulence-transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proc. Natl. Acad. Sci. USA 105 : 7489 7494. doi :.
110. Sabelis, M.W. Metz, J.A.J. 2002. Taking stock: relating theory to experiment. In : Adaptive Dynamics of Infectious Diseases: In Pursuit of Virulence Management (U. Dieckmann, J.A.J. Metz, M.W. Sabelis K. Sigmund, eds pp. 379 398. Cambridge University Press, Cambridge.
111. Sacristán, S. García-Arenal, F. 2008. The evolution of virulence and pathogenicity in plant pathogen populations. Mol. Plant. Biol. 9 : 369 384. doi :.
112. Salvaudon, L., Heraudet, V. Shykoff, J.A. 2005. Parasite-host fitness trade-offs change with parasite identity: genotype-specific interactions in a plant-pathogen system. Evolution 59 : 2518 2524. doi :.
113. Salvaudon, L., Heraudet, V. Shykoff, J.A. 2007. Genotype-specific interactions and the trade-off between host and parasite fitness. BMC Evol. Biol. 7 : 189 doi :.
114. Schjørring, S. Koella, J.C. 2003. Sub-lethal effects of pathogens can lead to the evolution of lower virulence in multiple infections. Proc. R. Soc. Lond. B 270 : 189 193. doi :.
115. Schmid-Hempel, P. 2008. Parasite immune evasion: a momentous molecular war. Trends Ecol. Evol. 23 : 318 326. doi :.
116. Smith, T. 1904. Some problems in the life-history of pathogenic microorganism. Science 20 : 817 832. doi :.
117. Svennungsen, T.O. Kisdi, I. 2009. Evolutionary branching of virulence in a single infection model. J. theor. Biol. in press.
118. Thomas, S.R. Elkinton, J.S. 2004. Pathogenicity and virulence. J. Invertebr. Pathol. 85 : 146 151. doi :.
119. Toft, C.A. Karter, A.J. 1990. Parasite-host coevolution. Trends Ecol. Evol. 5 : 326 329. doi :.
120. Topley, W.W.C. 1919. The spread of bacterial infection. Lancet 194 : 1 5. doi :.
121. Weiss, R.A. 2002. Virulence and pathogenesis. Trends Microbiol. 10 : 314 318. doi :.
122. West, S.A. Buckling, A. 2003. Cooperation, virulence and siderophore production in bacterial parasites. Proc. R. Soc. Lond. B 270 : 37 44. doi :.
123. Wickham, M.E., Brown, N.F., Boyle, E.C., Coombes, B.K. Finlay, B.B. 2007. Virulence is positively selected by transmission success between mammalian hosts. Curr. Biol. 17 : 783 788. doi :.