Experimental coevolution leads to a decrease in parasite-induced host mortality

Journal of Evolutionary Biology

Volumn 24, Issue 8, 2011, Pages 1777-1782

  Bérénos, Camillo ^a   Schmid Hempel, P ^a   Wegner, K M ^a,b,c  

^a ETH ZURICH   (Switzerland)

^b GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

^c ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

Author keywords

Adaptive evolution; Experimental evolution; Host parasite coevolution; Red queen hypothesis; Resistance

Indexed keywords

ADAPTATION; BEETLE; CLONAL ORGANISM; COEVOLUTION; EVOLUTIONARY BIOLOGY; EXPERIMENTAL STUDY; FUNGUS; HOST-PARASITE INTERACTION; LIFE HISTORY TRAIT; MORTALITY; OUTCROSSING; RED QUEEN HYPOTHESIS; VIRULENCE;

ANIMAL; ARTICLE; EVOLUTION; GENETICS; HOST PARASITE INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; MORTALITY; NOSEMA; PARASITOLOGY; PHYSIOLOGY; TRIBOLIUM;

ANIMALS; BIOLOGICAL EVOLUTION; HOST-PARASITE INTERACTIONS; IMMUNITY, INNATE; MORTALITY; NOSEMA; TRIBOLIUM;

MICROSPORIDIA; NOSEMA; NOSEMA WHITEI; TRIBOLIUM CASTANEUM;

EID: 79960239851     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2011.02306.x     Document Type: Article

References (50)

1. Adiba, S., Huet, M. & Kaltz, O. 2010. Experimental evolution of local parasite maladaptation. J. Evol. Biol. 23: 1195-1205.
2. Agrawal, A.F. & Otto, S.P. 2006. Host-parasite coevolution and selection on sex through the effects of segregation. Am. Nat. 168: 617-629.
3. Berenos, C., Schmid-Hempel, P. & Wegner, K.M. 2009. Evolution of host resistance and trade-offs between virulence and transmission potential in an obligately killing parasite. J. Evol. Biol. 22: 2049-2056.
4. Berenos, C., Wegner, K.M. & Schmid-Hempel, P. 2011. Antagonistic coevolution with parasites maintains host genetic diversity: an experimental test. Proc. R. Soc. B-Biol. Sci. 278: 218-224.
5. Blaser, M. & Schmid-Hempel, P. 2005. Determinants of virulence for the parasite Nosema whitei in its host Tribolium castaneum. J. Invertebr. Pathol. 89: 251-257.
6. Buckling, A. & Rainey, P.B. 2002. Antagonistic coevolution between a bacterium and a bacteriophage. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 269: 931-936.
7. 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.
8. Crow, J.F. & Kimura, M. 1965. Evolution in sexual and asexual populations. Am. Nat. 99: 439-450.
9. Decaestecker, E., Gaba, S., Raeymaekers, J.A.M., Stoks, R., Van Kerckhoven, L., Ebert, D. et al. 2007. Host-parasite 'Red Queen' dynamics archived in pond sediment. Nature 450: 870-U16.
10. Dunn, A.M. & Smith, J.E. 2001. Microsporidian life cycles and diversity: the relationship between virulence and transmission. Microbes Infect. 3: 381-388.
11. Ebert, D. 1994. Virulence and local adaptation of a horizontally transmitted parasite. Science 265: 1084-1086.
12. Ebert, D. 1998. Experimental evolution of parasites. Science 282: 1432-1435.
13. Fenner, F. & Cairns, J. 1959. Variation in virulence in relation to adaptation to new hosts. In: The Viruses, Vol. 3 (Burnet. FM & S. W, ed), pp. 225-249. Academic Press, New York.
14. Fischer, O. (2006) Host-Parasite Interactions and the Evolution of Meiotic Recombination in the Red Flour Beetle, Tribolium Castaneum (ETH thesis No. 16715). Eidgenössische Technische Hochschule ETH Zürich, Zuerich, pp. 181.
15. Fischer, O. & Schmid-Hempel, P. 2005. Selection by parasites may increase host recombination frequency. Biol. Lett. 1: 193-195.
16. Fisher, R.A. 1930. The Genetical Theory of Natural Selection. Clarendon Press, Oxford.
17. Forde, S.E., Thompson, J.N. & Bohannan, B.J.M. 2004. Adaptation varies through space and time in a coevolving host-parasitoid interaction. Nature 431: 841-844.
18. Gaba, S. & Ebert, D. 2009. Time-shift experiments as a tool to study antagonistic coevolution. Trends Ecol. Evol. 24: 226-232.
19. Gandon, S. & Michalakis, Y. 2002. Local adaptation, evolutionary potential and host-parasite coevolution: interactions between migration, mutation, population size and generation time. J. Evol. Biol. 15: 451-462.
20. Greischar, M.A. & Koskella, B. 2007. A synthesis of experimental work on parasite local adaptation. Ecol. Lett. 10: 418-434.
21. Hamilton, W.D. 1980. Sex versus non-sex versus parasite. Oikos 35: 282-290.
22. Jensen, K.H., Little, T., Skorping, A. & Ebert, D. 2006. Empirical support for optimal virulence in a castrating parasite. PLoS Biol. 4: 1265-1269.
23. Jokela, J., Dybdahl, M.F. & Lively, C.M. 2009. The maintenance of sex, clonal dynamics, and host-parasite coevolution in a mixed population of sexual and asexual snails. Am. Nat. 174: S43-S53.
24. Kopp, M. & Gavrilets, S. 2006. Multilocus genetics and the coevolution of quantitative traits. Evolution 60: 1321-1336.
25. Koskella, B. & Lively, C.M. 2007. Advice of the rose: experimental coevolution of a trematode parasite and its snail host. Evolution 61: 152-159.
26. Koskella, B. & Lively, C.M. 2009. Evidence for negative frequency-dependent selection during experimental coevolution of a freshwater snail and a sterilizing trematode. Evolution 63: 2213-2221.
27. Kouyos, R.D., Salathe, M. & Bonhoeffer, S. 2007. The Red Queen and the persistence of linkage-disequilibrium oscillations in finite and infinite populations. BMC Evol. Biol. 7: 211.
28. Legros, M. & Koella, J.C. 2010. Experimental evolution of specialization by a microsporidian parasite. BMC Evol. Biol. 10: 159.
29. Little, T.J. 2002. The evolutionary significance of parasitism: do parasite-driven genetic dynamics occur ex silico? J. Evol. Biol. 15: 1-9.
30. Lohse, K., Gutierrez, A. & Kaltz, O. 2006. Experimental evolution of resistance in Paramecium caudatum against the bacterial parasite Holospora undulata. Evolution 60: 1177-1186.
31. Mack, R.N., Simberloff, D., Mark Lonsdale, W., Evans, H., Clout, M. & Bazzaz, F.A. 2000. Biotic invasions: causes, epidemiology, global consequences, and control. Ecol. Appl. 10: 689-710.
32. Milner, R.J. 1972a. Nosema whitei, a microsporidan pathogen of some species of Tribolium 3: effect on Tribolium castaneum. J. Invertebr. Pathol. 19: 248-255.
33. Milner, R.J. 1972b. Nosema whitei, a Microsporidan pathogen of some species of Tribolium :1: morphology, life-cycle, and generation time. J. Invertebr. Pathol. 19: 231-238.
34. Milner, R.J. 1972c. Survival of Nosema whitei spores stored at 4 degrees C. J. Invertebr. Pathol. 20: 356-357.
35. Muskett, J.C., Reed, N.E. & Thornton, D.H. 1985. Increased virulence of an infectious Bursal disease live virus vaccine after passage in chicks. Vaccine 3: 309-312.
36. Nuismer, S.L. 2006. Parasite local adaptation in a geographic mosaic. Evolution 60: 24-30.
37. Peters, A.D. & Lively, C.M. 1999. The Red Queen and fluctuating epistasis: a population genetic analysis of antagonistic coevolution. Am. Nat. 154: 393-405.
38. R Development Core Team 2010. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
39. Ridenhour, B.J. & Nuismer, S.L. 2007. Polygenic traits and parasite local adaptation. Evolution 61: 368-376.
40. Roth, O., Joop, G., Eggert, H., Hilbert, J., Daniel, J., Schmid-Hempel, P. et al. 2009. Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum. J. Anim. Ecol. 79: 403-413.
41. Sadd, B.M., Kleinlogel, Y., Schmid-Hempel, R. & Schmid-Hempel, P. 2005. Trans-generational immune priming in a social insect. Biol. Lett. 1: 386-388.
42. Salathe, M., Kouyos, R.D., Regoes, R.R. & Bonhoeffer, S. 2008. Rapid parasite adaptation drives selection for high recombination rates. Evolution 62: 295-300.
43. Schulte, R.D., Makus, C., Hasert, B., Michiels, N.K. & Schulenburg, H. 2010. Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite. Proc. Natl. Acad. Sci. USA 107: 7359-7364.
44. Sokoloff, A. 1974. The Biology of TRIBOLIUM: vol. 2. Oxford University Press, Oxford.
45. Taylor, J.W., Jacobson, D.J. & Fisher, M.C. 1999. The evolution of asexual fungi: reproduction, speciation and classification. Annu. Rev. Phytopathol. 37: 197-246.
46. Wegner, K.M., Berenos, C. & Schmid-Hempel, P. 2008. Nonadditive genetic components in resistance of the red flour beetle Tribolium castanaeum against parasite infection. Evolution 62: 2381-2392a.
47. Wegner, K.M., Berenos, C. & Schmid-Hempel, P. 2009. Host genetic architecture in single and multiple infections. J. Evol. Biol. 22: 396-404.
48. Wilfert, L. & Schmid-Hempel, P. 2008. The genetic architecture of susceptibility to parasites. BMC Evol. Biol. 8: 187.
49. Woolhouse, M.E.J., 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.
50. Yourth, C.P. & Schmid-Hempel, P. 2006. Serial passage of the parasite Crithidia bombi within a colony of its host, Bombus terrestris, reduces success in unrelated hosts. Proc. R. Soc. B-Biol. Sci. 273: 655-659.