Temperature-dependent costs of parasitism and maintenance of polymorphism under genotype-by-environment interactions

Journal of Evolutionary Biology

Volumn 21, Issue 5, 2008, Pages 1418-1427

  Vale, P F ^a   Stjernman, M ^a,b   Little, T J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b LUND UNIVERSITY   (Sweden)

Author keywords

Cost of parasitism; Daphnia magna; Genetic variation; Genotype by environment interaction; Host parasite; Infectivity; Pasteuria ramosa; Temperature; Transmission; Virulence evolution

Indexed keywords

COEVOLUTION; CRUSTACEAN; ENVIRONMENTAL GRADIENT; FITNESS; GENETIC VARIATION; HOST-PARASITE INTERACTION; INFECTIVITY; PARASITISM; POLYMORPHISM; TEMPERATURE EFFECT; VIRULENCE;

ANIMAL; ARTICLE; DAPHNIA; FEMALE; GENETIC VARIABILITY; GENOTYPE; GRAM POSITIVE BACTERIUM; HOST PARASITE INTERACTION; MICROBIOLOGY; PHYSIOLOGY; STATISTICAL MODEL; TEMPERATURE;

ANIMALS; DAPHNIA; FEMALE; GENETIC VARIATION; GENOTYPE; GRAM-POSITIVE ENDOSPORE-FORMING BACTERIA; HOST-PARASITE INTERACTIONS; LINEAR MODELS; TEMPERATURE;

CRUSTACEA; DAPHNIA; DAPHNIA MAGNA; PASTEURIA RAMOSA;

EID: 49549086827     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2008.01555.x     Document Type: Article

References (58)

1. Anderson, R.M. May, R.M. 1982. Coevolution of hosts and parasites. Parasitology (Pt 2) 85 : 411 426.
2. 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.
3. Bedhomme, S., Agnew, P., Sidobre, C. Michalakis, Y. 2004. Virulence reaction norms across a food gradient. Proc. R. Soc. Lond. B 271 : 739 744.
4. Bell, G.A.C. 1997. Experimental evolution in Chlamydomonas. 1. Short-term selection in uniform and diverse environments. Heredity 78 : 490 497.
5. Bell, G. Reboud, X. 1997. Experimental evolution in Chlamydomonas. 2. Genetic variation in strongly contrasted environments. Heredity 78 : 498 506.
6. Ben-Ami, F., Regoes, R.R. Ebert, D. 2008. A quantitative test of the relationship between parasite dose and infection probability across different host-parasite combinations. Proc. R. Soc. Lond. B 275 : 853 859.
7. Blanford, S., Thomas, M.B., Pugh, C. Pell, J.K. 2003. Temperature checks the Red Queen? Resistance and virulence in a fluctuating environment Ecol. Lett. 6 : 2 5.
8. Bremermann, H.J. Pickering, J. 1983. A game-theoretical model of parasite virulence. J. Theor. Biol. 100 : 411 426.
9. Byers, D.L. 2005. Evolution in heterogeneous environments and the potential of maintenance of genetic variation in traits of adaptive significance. Genetica 123 : 107 124.
10. Carius, H.J., Little, T.J. Ebert, D. 2001. Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution 55 : 1136 1145.
11. Carvallo, G.R. 1987. The clonal ecology of Daphnia magna (Crustacea: Cladocera). 2. Thermal differentiation among seasonal clones. J. Anim. Ecol 56 : 469 478.
12. Day, T. 2004. A general theory for the evolutionary dynamics of virulence. Am. Nat. 163 : E40 E63.
13. Decaestecker, E., Gaba, S., Raeymaekers, J.A., Stoks, R., Van Kerckhoven, L., Ebert, D. De Meester, L. 2007. Host-parasite 'Red Queen' dynamics archived in pond sediment. Nature 450 : 870 873.
14. Duncan, A.B. Little, T.J. 2007. Parasite-driven genetic change in a natural population of Daphnia. Evolution 61 : 796 803.
15. Ebert, D. 2004. The evolution of virulence when parasites cause host castration and gigantism. Am. Nat. 164 (Suppl.5 S19 S32.
16. Ebert, D. Weisser, W.W. 1997. Optimal killing for obligate killers: the evolution of life histories and virulence of semelparous parasites. Proc. R. Soc. Lond. B 264 : 985 991.
17. Ebert, D., Yampolsky, L. Stearns, S.C. 1993. Genetics of life-history in Daphnia magna. 1. Heritabilities at 2 food levels. Heredity 70 : 335 343.
18. Ebert, D., Rainey, P., Embley, T.M. Scholz, D. 1996. Development, life cycle, ultrastructure and phylogenetic position of Pasteuria ramosa Metchnikoff 1888: rediscovery of an obligate endoparasite of Daphnia magna Straus. Philos. Trans. R. Soc. Lond. B 351 : 1689 1701.
19. Ebert, D., Zschokke-Rohringer, C.D. Carius, H.J. 2000. Dose effects and density-dependent regulation of two microparasites of Daphnia magna. Oecologia 122 : 200 209.
20. Ebert, D., Carius, H.J., Little, T. Decaestecker, E. 2004. The evolution of virulence when parasites cause host castration and gigantism. Am. Nat. 164 : S19 S32.
21. Falconer, D.S. 1952. The problem of environment and selection. Am. Nat. 86 : 293 298.
22. Falconer, D.S. Latyszewski, M. 1952. The environment in relation to selection for size in mice. J. Genet. 51 : 67 80.
23. Falconer, D.S. Mackay, T.D.S. 1996. Introduction to Quantitative Genetics, 4th edn. Longmans Green, Harlow, Essex, UK.
24. Fels, D. Kaltz, O. 2006. Temperature-dependent transmission and latency of Holospora undulata, a micronucleus-specific parasite of the ciliate Paramecium caudatum. Proc. R. Soc. Lond. B 273 : 1031 1038.
25. Ferguson, H.M. Read, A.F. 2002. Genetic and environmental determinants of malaria parasite virulence in mosquitoes. Proc. R. Soc. Lond. B 269 : 1217 1224.
26. Frank, S.A. 1996. Models of parasite virulence. Q. Rev. Biol. 71 : 37 78.
27. Galvani, A.P. 2003. Epidemiology meets evolutionary ecology. Trends Ecol. Evol. 18 : 132 139.
28. Gandon, S., Mackinnon, M.J., Nee, S. Read, A.F. 2001. Imperfect vaccines and the evolution of pathogen virulence. Nature 414 : 751 756.
29. Gillespie, J.H. Turelli, M. 1989. Genotype-environment interactions and the maintenance of polygenic variation. Genetics 121 : 129 138.
30. Grenfell, B.T., Pybus, O.G., Gog, J.R., Wood, J.L., Daly, J.M., Mumford, J.A. Holmes, E.C. 2004. Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303 : 327 332.
31. Haldane, J.B.S. 1949. Disease and evolution. Ric. Sci. Suppl. 19 : 68 76.
32. Jensen, K.H., Little, T., Skorping, A. Ebert, D. 2006. Empirical support for optimal virulence in a castrating parasite. PLoS Biol. 4 : e197.
33. Kluttgen, B., Dulmer, U., Engels, M. Ratte, H.T. 1994. ADaM, an artificial fresh-water for the culture of zooplankton. Water Res. 28 : 743 746.
34. Laine, A.L. 2007. Pathogen fitness components and genotypes differ in their sensitivity to nutrient and temperature variation in a wild plant-pathogen association. J. Evol. Biol. 20 : 2371 2378.
35. Lambrechts, L., Chavatte, J.M., Snounou, G. Koella, J.C. 2006. Environmental influence on the genetic basis of mosquito resistance to malaria parasites. Proc. R. Soc. Lond. B 273 : 1501 1506.
36. Lampert, W. 1987. Feeding and nutrition in Daphnia. In: Daphnia R. H. Peters R. de Bernardi, eds). Men. Ist. Ital. Idrobiol. 45 : 143 192.
37. Levene, H. 1953. Genetic equilibrium when more than one ecological niche is available. Am. Nat. 87 : 331 333.
38. Little, T.J. Ebert, D. 1999. Associations between parasitism and host genotype in natural populations of Daphnia (Crustacea: Cladocera). J. Anim, Ecol 68 : 134 149.
39. Little, T.J. Ebert, D. 2000. The cause of parasitic infection in natural population of Daphnia (Crustacea: Cladocera): the role of host genetics. Proc. R. Soc. Lond. B 267 : 2037 2042.
40. Little, T.J. Killick, S.C. 2007. Evidence for a cost of immunity when the crustacean Daphnia magna is exposed to the bacterial pathogen Pasteuria ramosa. J. Anim. Ecol. 76 : 1202 1207.
41. Little, T., Birch, J., Vale, P. Tseng, M. 2007a. Parasite transgenerational effects on infection. Evol. Ecol. Res. 9 : 459 469.
42. Little, T.J., Chadwick, W. Watt, K. 2007b. Parasite variation and the evolution of virulence in a Daphnia-microparasite system. Parasitology 35 : 303 308.
43. Lively, C.M. 1989. Adaptation by a parasitic trematode to local-populations of its snail host. Evolution 43 : 1663 1671.
44. Maynard Smith, J. Hoekstra, R. 1980. Polymorphism in a varied environment: how robust are the models. Genet. Res. 35 : 45 57.
45. Mitchell, S.E. Read, A.F. 2005. Poor maternal environment enhances offspring disease resistance in an invertebrate. Proc. R. Soc. Lond. B 272 : 2601 2607.
46. Mitchell, S.E., Rogers, E.S., Little, T.J. Read, A.F. 2005. Host-parasite and genotype-by-environment interactions: temperature modifies potential for selection by a sterilizing pathogen. Evolution 59 : 70 80.
47. Mouton, L. Ebert, D. 2008. Variable-number-of-tandem-repeats analysis of genetic diversity in Pasteuria ramosa. Curr. Microbiol. 56 : 447 452.
48. Mouton, L., Nong, G., Preston, J.F. Ebert, D. 2007. Variable-number tandem repeats as molecular markers for biotypes of Pasteuria ramosa in Daphnia spp. Appl. Environ. Microbiol. 73 : 3715 3718.
49. Regoes, R.R., Hottinger, J.W., Sygnarski, L. Ebert, D. 2003. The infection rate of Daphnia magna by Pasteuria ramosa conforms with the mass-action principle. Epidemiol. Infect. 131 : 957 966.
50. Restif, O. Kaltz, O. 2006. Condition-dependent virulence in a horizontally and vertically transmitted bacterial parasite. Oikos 114 : 148 158.
51. 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.
52. 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.
53. Sasaki, A. de Jong, G. 1999. Density dependence and unpredictable selection in a heterogeneous environment: Compromise and polymorphism in the ESS reaction norm. Evolution 53 : 1329 1342.
54. Sgro, C.M. Hoffmann, A.A. 2004. Genetic correlations, tradeoffs and environmental variation. Heredity 93 : 241 248.
55. Stearns, S.C. 1976. Life-history tactics: a review of the ideas. Q. Rev. Biol. 51 : 3 47.
56. Takala, S.L., Coulibaly, D., Thera, M.A., Dicko, A., Smith, D.L., Guindo, A.B., Kone, A.K., Traore, K., Ouattara, A., Djimde, A.A., Sehdev, P.S., Lyke, K.E., Diallo, D.A., Doumbo, O.K. Plowe, C.V. 2007. Dynamics of polymorphism in a malaria vaccine antigen at a vaccine-testing site in Mali. PLoS Med. 4 : e93.
57. Wolinska, J., Bittner, K., Ebert, D. Spaak, P. 2006. The coexistence of hybrid and parental Daphnia: the role of parasites. Proc. R. Soc. Lond. B 273 : 1977 1983.
58. Woolhouse, M.E., Webster, J.P., Domingo, E., Charlesworth, B. Levin, B.R. 2002. Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat. Genet. 32 : 569 577.