Experimental evolution of resistance in Paramecium caudatum against the bacterial parasite Holospora undulata

Evolution

Volumn 60, Issue 6, 2006, Pages 1177-1186

  Lohse, Konrad ^a   Gutierrez, Arnaud ^b   Kaltz, Oliver ^b  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b Laboratoire de Parasitologie Evolutive CNRS UMR 7103 UFR 927   (France)

Author keywords

Coevolution; Costs of resistance; Cross infection; Infectivity; Local adaptation

Indexed keywords

ADAPTATION; BACTERIUM; COEVOLUTION; FITNESS; GENOTYPE; LIFE HISTORY TRAIT; PARASITE RESISTANCE;

BACTERIA (MICROORGANISMS); HOLOSPORA; HOLOSPORA UNDULATA; PARAMECIUM CAUDATUM; PROTOZOA;

ANIMAL; ARTICLE; DIRECTED MOLECULAR EVOLUTION; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; GENOTYPE; HOLOSPORACEAE; HOST PARASITE INTERACTION; METHODOLOGY; MICROBIOLOGY; PARAMECIUM CAUDATUM; PHYSIOLOGY;

ANIMALS; DIRECTED MOLECULAR EVOLUTION; GENOTYPE; HOLOSPORACEAE; HOST-PARASITE RELATIONS; PARAMECIUM CAUDATUM; SELECTION (GENETICS); VARIATION (GENETICS);

EID: 33748575275     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1554/05-656.1     Document Type: Article

References (73)

1. Agrawal, A. F., and C. M. Lively. 2002. Infection genetics: gene-for-gene versus matching-alleles models and all points in between. Evol. Ecol. Res. 4:79-90.
2. Amann, R., N. Springer, W. Ludwig, H.-D. Görtz, and K.-H. Schlaifer. 1991. Identification in situ and phylogeny of uncultured bacterial endosymbionts. Nature 351:161-164.
3. 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 257:105-110.
4. Bell, G., and J. Maynard Smith. 1987. Short-term selection for recombination among mutually antagonistic species. Nature 328:66-68.
5. Bergelson, J., G. Dwyer, and J. Emerson. 2001. Models and data on plant-enemy coevolution. Annu. Rev. Genet. 35:469-499.
6. Boots, M., and M. Begon. 1993. Trade-offs with resistance to a granulovirus in the Indian meal moth examined by a laboratory evolution experiment. Funct. Ecol. 7:528-534.
7. Boulétreau, M. 1986. The genetic and coevolutionary interactions between parasitoids and their hosts. Pp. 160-200 in J. Waage and D. Greathead, eds. Insect parasitoids. Academic Press, London.
8. Brockhurst, M. A., A. D. Morgan, P. B. Rainey, and A. Buckling. 2004. Population mixing accelerates coevolution. Ecol. Lett. 6:975-979.
9. Brown, J. K. 2003. A cost of disease resistance: paradigm or peculiarity? Trends Genet. 19:667-671.
10. Buckling, A., and P. B. Rainey. 2002a. Antagonistic coevolution between a bacterium and a bacteriophage. Proc. R. Soc. Lond. B 269:931-936.
11. _. 2002b. The role of parasites in sympatric and allopatric host diversification. Nature 420:496-499.
12. Burdon, J. J. 1987. Diseases and plant population biology. Cambridge Univ. Press, Cambridge, U.K.
13. Capaul, M., and D. Ebert. 2003. Parasite-mediated selection in experimental Daphnia magna populations. Evolution 57:249-260.
14. Carius, H. J., T. J. Little, and D. Ebert. 2001. Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution 55:1136-1145.
15. Chao, L., B. R. Levin, and F. M. Stewart. 1977. A complex community in a simple habitat: an experimental study with bacteria and phage. Ecology 58:369-378.
16. Coustau, C., C. Chevillon, and R. Ffrench-Constant. 2000. Resistance to xenobiotics and parasites: Can we count the cost? Trends Ecol. Evol. 15:378-383.
17. Crawley, M. J. 1993. GLIM for ecologists. Blackwell Scientific Publications, Oxford, U.K.
18. De Wit, P. J. G. M. 1997. Pathogen avirulence and plant resistance: a key role for recognition. Trends Plant Sci. 2:452-458.
19. Ebert, D. 1998. Experimental evolution of parasites. Science 282:1432-1435.
20. Ebert, D., and W. D. Hamilton. 1996. Sex against virulence: the coevolution of parasitic diseases. Trends Ecol. Evol. 11:79-82.
21. Ebert, D., and K. L. Mangin. 1997. The influence of host demography on the evolution of virulence of a microsporidian gut parasite. Evolution 51:1828-1837.
22. Elena, S. F. 2001. Evolutionary history conditions the timing of transmission in vesicular stomatitis virus. Infect. Genet. Evol. 1:151-159.
23. Fels, D., and O. Kaltz. 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.
24. Fischer, O., and P. Schmid-Hempel. 2005. Selection by parasites may increase host recombination frequency. Biol. Lett. 1:193-195.
25. Fokin, S. I. 2004. Bacterial endocytobionts of ciliophora and their interactions with the host cell. Int. Rev. Cytol. 236:181-249.
26. Fokin, S. I., and I. N. Skovorodkin. 1997. Experimental analysis of the resistance of Paramecium caudatum (Ciliophora) against infection by bacterium Holospora undulata. Eur. J. Protistol. 33:214-218.
27. Fokin, S. I., T. Brigge, J. Brenner, and H.-D. Görtz. 1996. Holospora species infecting the nuclei of Paramecium appear to belong into two groups of bacteria. Eur. J. Protistol. 32:SI19-24.
28. Fokin, S. I., I. N. Skovorodkin, and E. V. Sabaneyeva. 2003. Initial steps of infection of the ciliate Paramecium with bacteria Holospora sp. tsitologiia 45:1227-1233.
29. Forde, S. E., J. N. Thompson, and B. J. Bohannan. 2004. Adaptation varies through space and time in a coevolving host-parasitoid interaction. Nature 431:841-844.
30. Frank, S. A. 1991. Ecological and genetic models of host-pathogen coevolution. Heredity 67:73-83.
31. _. 1994. Recognition and polymorphism in host-parasite genetics. Philos. Trans. R. Soc. Lond. B 346:283-293.
32. Freiburg, M. 1988. Organization and expression of the nuclear genome. Pp. 141-154 in H.-D. Görtz, ed. Paramecium. Springer-Verlag, Berlin.
33. Gandon, S. 2002. Local adaptation and the geometry of host-parasite coevolution. Ecol. Lett. 5:246-256.
34. Görtz, H.-D. 1988. Paramecium. Springer, Berlin.
35. Görtz, H.-D., and T. Brigge. 1998. Intracellular bacteria in protozoa. Naturwissenschaften 85:359-368.
36. Görtz, H.-D., and J. Dieckmann. 1980. Life cycle and infectivity of Holospora elegans Haffkine, a micronucleus-specific symbiont of Paramecium caudatum (Ehrenberg). Protistologia 16:591-603.
37. Görtz, H.-D., and M. Wiemann. 1989. Route of infection of the bacteria Holospora elegans and Holospora obtusa into the nuclei of Paramecium caudatum. Eur. J. Protistol. 24:101-109.
38. Haag, C. R., and D. Ebert. 2004. Parasite-mediated selection in experimental metapopulations of Daphnia magna. Proc. R. Soc. Lond. B 271:2149-2155.
39. Haldane, J. B. S. 1949. Disease and evolution. Ric. Sci. 19:68-76.
40. Hamilton, W. D. 1980. Sex versus non-sex versus parasite. Oikos 35:282-290.
41. Kaltz, O., and T. Nidelet. 2004. Experimental evolution of host x parasite genotype interactions. Workshop on Experimental Evolution, University of Fribourg, Switzerland.
42. Kaltz, O., and J. A. Shykoff. 1998. Local adaptation in host-parasite systems. Heredity 81:361-370.
43. _. 2002. Within- and among-population variation in infectivity, latency and spore production in a host-pathogen system. J. Evol. Biol. 15:850-860.
44. Kraaijeveld, A. R., and H. C. Godfray. 1997. Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389:278-280.
45. Lambrechts, L., J. Halbert, P. Durand, L. C. Gouagna, and J. C. Koella. 2005. Host genotype by parasite genotype interactions underlying the resistance of anopheline mosquitoes to Plasmodium falciparum. Malaria J. 4:3-11.
46. Lenski, R. E., and B. R. Levin. 1985. Constraints on the coevolution of bacteria and virulent phage: a model, some experiments, and predictions for natural communities. Am. Nat. 125:585-602.
47. Little, T. J. 2002. The evolutionary significance of parasitism: Do parasite-driven genetic dynamics occur ex silico? J. Evol. Biol. 15:1-9.
48. Lively, C. M., E. J. Lyons, A. D. Peters, and J. Jokela. 1998. Environmental stress and the maintenance of sex in a freshwater snail. Evolution 52:1482-1486.
49. Mackinnon, M. J., and A. F. Read. 1999. Selection for high and low virulence in the malaria parasite Plasmodium chabaudi. Proc. R. Soc. Lond. B 266:741-748.
50. Messenger, S., I. Molineux, and J. Bull. 1999. Virulence evolution in a virus obeys a trade-off. Proc. R. Soc. Lond. B 266:397-404.
51. Morand, S., S. D. Manning, and M. E. Woolhouse. 1996. Parasite-host coevolution and geographic patterns of parasite infectivity and host susceptibility. Proc. R. Soc. Lond. B 263:119-128.
52. Morgan, A. D., S. Gandon, and A. Buckling. 2005. The effect of migration on local adaptation in a coevolving host-parasite system. Nature 437:253-256.
53. Nee, S. 1989. Antagonistic coevolution and the evolution of genotypic randomization. J. Theor. Biol. 140:499-518.
54. Parker, M. A. 1994. Pathogens and sex in plants. Evol. Ecol. 8:560-584.
55. Rausher, M. D. 1996. Genetic analysis of coevolution between plants and their natural enemies. Trends Genet. 12:212-217.
56. Restif, O., and O. Kaltz. 2006. Condition-dependent virulence in a horizontally and vertically transmitted bacterial parasite. Oikos in press.
57. Rigby, M. C., R. F. Hechinger, and L. Stevens. 2002. Why should parasite resistance be costly? Trends Parasitol. 18:116-120.
58. SAS. 1996. SAS/STAT user's guide. Release 6.11. SAS Institute, Cary, NC.
59. _. 2003. JMP statistics and graphics guide. Ver. 5.0.1.2. SAS Institute, Cary, NC.
60. Schmid, B., and C. Dolt. 1994. Effects of maternal and paternal environment and genotype on offspring phenotype in Solidago altissima L. Evolution 48:1525-1549.
61. Simms, E. L., and J. Triplett. 1994. Costs and benefits of plant responses to disease: resistance and tolerance. Evolution 48:1973-1985.
62. Sorci, G., A. P. Møller, and T. Boulinier. 1997. Genetics of host-parasite interactions. Trends Ecol. Evol. 12:196-200.
63. Stewart, A. D., J. M. Logsdon, Jr.,and S. E. Kelley. 2005. An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution 59:730-739.
64. Strauss, S. Y., J. A. Rudgers, J. A. Lau, and R. E. Irwin. 2002. Direct and ecological costs of resistance to herbivory. Trends Ecol. Evol. 17:278-285.
65. Thompson, J. N. 1994. The coevolutionary process. Univ. of Chicago Press, Chicago.
66. _. 1999. Specific hypotheses on the geographic mosaic of coevolution. Am. Nat. 153:S1-S14.
67. Thrall, P. H., and J. J. Burdon. 2003. Evolution of virulence in a plant host-pathogen metapopulation. Science 299:1735-1737.
68. Turner, P. E., and L. Chao. 1999. Prisoner's dilemma in an RNA virus. Nature 398:441-443.
69. Van Zandt, P. A., and S. Mopper. 1998. A meta-analysis of the adaptive deme formation analysis in phytophagous insect populations. Am. Nat. 152:595-604.
70. Webster, J. P., and M. E. J. Woolhouse. 1999. Cost of resistance: relationship between reduced fertility and increased resistance in a Schistosoma host-parasite system. Proc. R. Soc. Lond. B 266:391-396.
71. Webster, J. P., C. M. Gower, and L. Blair. 2004. Do hosts and parasites coevolve? Empirical support from the Schistosoma system. Am. Nat. 164S:S34-S51.
72. Wichtermann, R. T. 1986. The biology of Paramecium. Plenum Press, New York.
73. Woolhouse, M. E., 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.