Experimental evolution shows Drosophila melanogaster resistance to a microsporidian pathogen has fitness costs

Evolution

Volumn 63, Issue 1, 2009, Pages 104-114

  Vijendravarma, Roshan K ^a,b   Kraaijeveld, Alex R ^a,c   Godfray, H C J ^a,d  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Drosophila; Experimental evoluation; Invertebrate immunity; Microsporidia; Parasite; Resistance

Indexed keywords

COMPARATIVE STUDY; DISEASE RESISTANCE; EVOLUTION; EXPERIMENTAL STUDY; FECUNDITY; FITNESS; FLY; IMMUNE SYSTEM; LONGEVITY; PARASITE;

ANIMAL; ARTICLE; BLOOD CELL; DROSOPHILA MELANOGASTER; EVOLUTION; FERTILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; LARVA; MICROBIOLOGY; MICROSPORIDA; PARASITOLOGY;

ANIMALS; DROSOPHILA MELANOGASTER; EVOLUTION; FERTILITY; HEMOCYTES; LARVA; MICROSPORIDA;

ACARI; BACTERIA (MICROORGANISMS); DROSOPHILA MELANOGASTER; INVERTEBRATA; MICROSPORIDIA; TUBULINOSEMA KINGI;

EID: 58249106874     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2008.00516.x     Document Type: Article

References (100)

1. Agrawal, A., 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. Anderson, R. M., and R. M. May. 1982. Coevolution of hosts and parasites. Parasitology 85 : 411 426.
3. Andreadis, T. G. 2007. Microsporidian parasites of mosquitoes. J. Am. Mosquito Contr. 23 : 3 29.
4. 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.
5. Armstrong, E. 1976. Transmission and infectivity studies on Nosema kingi in Drosophila willistoni and other drosophilids. Zeit. Parasitenkd. 50 : 161 165.
6. Armstrong, E., and L. Bass. 1989a. Effects of Nosema kingi on the development and weight of adult Drosophila melanogaster (OR-R-Strain). J. Invertebr. Pathol. 53 : 102 106.
7. Armstrong, E., and L. Bass. 1989b. Nosema kingi: effects on fecundity, fertility, and longevity of Drosophila melanogaster. J. Exp. Zool. 250 : 82 86.
8. Armstrong, E., L. Bass, K. Staker, and L. Harrell. 1986. A comparison of the biology of a Nosema in Drosophila melanogaster to Nosema kingi in Drosophila willistoni. J. Invertebr. Pathol. 48 : 124 126.
9. Bergelson, J., C. B. Purrington, C. J. Palm, and J.-C. Lopez-Gutierrez. 1996. Costs of resistance: a test using transgenic Arabidopsis thaliana. Proc. R. Soc. Lond. B 263 : 1659 1663.
10. Biron, D. G., P. Agnew, L. Marche, L. Renault, C. Sidobre, and Y. Michalakis. 2005. Proteome of Aedes aegypti larvae in response to infection by the intracellular parasite Vavraia culicis. Int. J. Parasitol. 35 : 1385 1397.
11. Bischoff, V., C. Vignal, B. Duvic, I. G. Boneca, J. A. Hoffmann, and J. Royet. 2006. Downregulation of the Drosophila immune response by peptidoglycan-recognition proteins SC1 and SC2. Plos Pathog. 2 : 139 147.
12. Boots, M., and M. Begon. 1993. Trade-offs with resistance to a granulosis virus in the Indian Meal Moth, examined by a laboratory evolution experiment. Funct. Ecol. 7 : 528 534.
13. Brown, J. K. M. 2003. A cost of disease resistance: paradigm or peculiarity Trends Genet. 19 : 667 671.
14. Brun, G., and N. Plus. 1980. The viruses of Drosophila. Pp. 625 702 in M. Ashburner, and T. R. F. Wright, eds. The genetics and biology of Drosophila. Academic Press, New York.
15. Buckling, A., and P. B. Rainey. 2002. Antagonistic coevolution between a bacterium and a bacteriophage. Proc. R. Soc. Lond. B 269 : 931 936.
16. Capaul, M., and D. Ebert. 2003. Parasite-mediated selection in experimental Daphnia magna populations. Evolution 57 : 249 260.
17. Carton, Y., and M. B. Sokolowski. 1992. Interactions between searching strategies of Drosophila parasitoids and the polymorphic behaviour of their hosts. J. Insect Behav. 5 : 161 175.
18. Carton, Y., F. Chibani, S. Haouas, and M. Marrakchi. 1987. Egg-laying strategy under natural conditions of Leptopilina boulardi, a hymenopteran parasitoid of Drosophila spp. Entomol. Exp. Appl. 43 : 193 201.
19. Carton, Y., S. Haouas, M. Marrakchi, and M. Hochberg. 1991. Two competing parasitoid species coexist in sympatry. Oikos 60 : 222 230.
20. 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.
21. Combes, C. 2001. Parasitism, the ecology & evolution of intimate interactions. Chicago Univ. Press, Chicago.
22. Contamine, D., A. M. Petitjean, and M. Ashburner. 1989. Genetic resistance to viral infection - the molecular cloning of a Drosophila gene that restricts infection by the Rhabdovirus Sigma. Genetics 123 : 525 533.
23. Corby-Harris, V., and D. E. L. Promislow. 2008. Host ecology shapes geographical variation for resistance to bacterial infection in Drosophila melanogaster. J. Anim. Ecol. 77 : 768 776.
24. Dubuffet, A., S. Dupas, F. Frey, J. M. Drezen, M. Poirie, and Y. Carton. 2007. Genetic interactions between the parasitoid wasp Leptopilina boulardi and its Drosophila hosts. Heredity 98 : 21 27.
25. Dunn, A. M., and J. E. Smith. 2001. Microsporidian life cycles and diversity: the relationship between virulence and transmission. Microbes Infect. 3 : 381 388.
26. Dunn, A. M., R. S. Terry, and J. E. Smith. 2001. Transovarial transmission in the Microsporidia. Adv. Parasitol. 48 : 57 100.
27. Dupas, S., and Y. Carton. 1999. Two non-linked genes for specific virulence of Leptopilina boulardi against Drosophila melanogaster and D. yakuba. Evol. Ecol. 13 : 211 220.
28. Dupas, S., Y. Carton, and M. Poirie. 2003. Genetic dimension of the coevolution of virulence-resistance in Drosophila - parasitoid wasp relationships. Heredity 90 : 84 89.
29. Fellowes, M. D. E., and H. C. J. Godfray. 2000. The evolutionary ecology of resistance to parasitoids by Drosophila. Heredity 84 : 1 8.
30. Fellowes, M. D. E., A. R. Kraaijeveld, and H. C. J. Godfray. 1998. Trade-off associated with selection for increased ability to resist parasitoid attack in Drosophila melanogaster. Proc. R. Soc. Lond. B 265 : 1553 1558.
31. Fellowes, M. D. E., A. R. Kraaijeveld, and H. C. J. Godfray. 1999a. Association between feeding rate and parasitoid resistance in Drosophila melanogaster. Evolution 53 : 1302 1305.
32. Fellowes, M. D. E., A. R. Kraaijeveld, and H. C. J. Godfray. 1999b. Cross-resistance following artificial selection for increased defense against parasitoids in Drosophila melanogaster. Evolution 53 : 966 972.
33. Fellowes, M. D. E., A. R. Kraaijeveld, and H. C. J. Godfray. 1999c. The relative fitness of Drosophila melanogaster (Diptera, Drosophilidae) that have successfully defended themselves against the parasitoid Asobara tabida (Hymenoptera, Braconidae). J. Evol. Biol. 12 : 123 128.
34. Ferrari, J., C. B. Muller, A. R. Kraaijeveld, and H. C. J. Godfray. 2001. Clonal variation and covariation in aphid resistance to parasitoids and a pathogen. Evolution 55 : 1805 1814.
35. Fleury, F., N. Ris, R. Allemand, P. Fouillet, Y. Carton, and M. Bouletreau. 2004. Ecological and genetic interactions in Drosophila parasitoids communities: a case study with D. melanogaster, D. simulans and their common Leptopilina parasitoids in south-eastern France. Genetica 120 : 181 194.
36. Franzen, C., P. H. Futerman, J. Schroeder, B. Salzberger, and A. R. Kraaijeveld. 2006. An ultrastructural and molecular study of Tubulinosema kingi Kramer (Microsporidia: Tubulinosematidae) from Drosophila melanogaster (Diptera: Drosophilidae) and its parasitoid Asobara tabida (Hymenoptera: Braconidae). J. Invertebr. Pathol. 91 : 158 167.
37. Futerman, P. H., S. J. Layen, M. L. Kotzen, C. Franzen, A. R. Kraaijeveld, and H. C. J. Godfray. 2006. Fitness effects and transmission routes of a microsporidian parasite infecting Drosophila and its parasitoids. Parasitology 132 : 479 492.
38. Gemmill, A. W., and A. F. Read. 1998. Counting the costs of disease resistance. Trends Ecol. Evol. 13 : 8 9.
39. Godfray, H. C. J. 1994. Parasitoids, behavioral and evolutionary ecology. Princeton Univ. Press, Princeton, NJ.
40. Goss, E. M., and J. Bergelson. 2006. Variation in resistance and virulence in the interaction between Arabidopsis thaliana and a bacterial pathogen. Evolution 60 : 1562 1573.
41. Haag, C. R., and D. Ebert. 2004. Parasite-mediated selection in experimental metapopulations of Daphnia magna. Proc. R. Soc. Lond. B 271 : 2149 2155.
42. Haldane, J. B. S. 1949. Disease and evolution. La Ricerca Scientifica 19 : S68 S76.
43. Hibbett, D. S., M. Binder, J. F. Bischoff, M. Blackwell, P. F. Cannon, O. E. Eriksson, S. Huhndorf, T. James, P. M. Kirk, R. Lucking, et al. 2007. A higher-level phylogenetic classification of the Fungi. Mycol. Res. 111 : 509 547.
44. Hirt, R. P., J. M. Logsdon, B. Healy, M. W. Dorey, W. F. Doolittle, and T. M. Embley. 1999. Microsporidia are related to Fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc. Natl. Acad. Sci. USA 96 : 580 585.
45. Hoch, G., L. F. Solter, and A. Schopf. 2004. Hemolymph melanization and alterations in hemocyte numbers in Lymantria dispar larvae following infections with different entomopathogenic microsporidia. Entomol. Exp. Appl. 113 : 77 86.
46. Hultmark, D. 2003. Drosophila immunity: paths and patterns. Curr. Opin. Immunol. 15 : 12 19.
47. Hurd, H., P. J. Taylor, D. Adams, A. Underhill, and P. Eggleston. 2005. Evaluating the costs of mosquito resistance to malaria parasites. Evolution 59 : 2560 2572.
48. Jaenike, J. 2000. Effectively vertical transmission of a Drosophila-parasitic nematode: mechanism and consequences. Ecol. Entomol. 25 : 395 402.
49. Jaenike, J., and I. Dombeck. 1998. General-purpose genotypes for host species utilization in a nematode parasite of Drosophila. Evolution 52 : 832 840.
50. James, T. Y., F. Kauff, C. L. Schoch, P. B. Matheny, V. Hofstetter, C. J. Cox, G. Celio, C. Gueidan, E. Fraker, J. Miadlikowska, et al. 2006. Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443 : 818 822.
51. Kraaijeveld, A. R., and H. C. J. Godfray. 1997. Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389 : 278 280.
52. Kraaijeveld, A. R., and H. C. J. Godfray. 1999. Geographic patterns in the evolution of resistance and virulence in Drosophila and its parasitoids. Am. Nat. 153 : S61 S74.
53. Kraaijeveld, A. R., and H. C. J. Godfray. 2008. Selection for resistance to a fungal pathogen in Drosophila melanogaster. Heredity 100 : 400 406.
54. Kraaijeveld, A. R., and J. J. M. van Alphen. 1994. Geographical variation in resistance of the parasitoid Asobara tabida against encapsulation by Drosophila melanogaster larvae: the mechanism explored. Physiol. Entomol. 19 : 9 14.
55. Kraaijeveld, A. R., E. C. Limentani, and H. C. J. Godfray. 2000. Basis of trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Proc. R. Soc. Lond. B 268 : 259 262.
56. Kramer, J. P. 1964. Nosema kingi sp. n., a microsporidian from Drosophila willistoni Sturtevant, and its infectivity for other muscoids. J. Insec. Path. 6 : 491 499.
57. Kurtz, J., A. A. Nahif, and K. P. Sauer. 2000. Phagocytosis of Vairimorpha sp (Microsporida, Nosematidae) spores by Plutella xylostella and Panorpa vulgaris hemocytes. J. Invertebr. Pathol. 75 : 237 239.
58. Laigo, F. M., and J. D. Paschke. 1966. Variations in total haemocyte counts as induced by a nosemosis in the cabbage looper, Trichoplusia ni. J. Invertebr. Pathol. 8 : 175 179.
59. Lazzaro, B. P., B. K. Sceurman, and A. G. Clark. 2004. Genetic basis of natural variation in Drosophila melanogaster antibacterial immunity. Science 303 : 1873 1876.
60. Lazzaro, B. P., T. B. Sackton, and A. G. Clark. 2006. Genetic variation in Drosophila melanogaster resistance to infection: a comparison across bacteria. Genetics 174 : 1539 1554.
61. Lemaitre, B., and J. Hoffmann. 2007. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25 : 697 743.
62. 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.
63. Leulier, F., C. Parquet, S. Pili-Floury, J. H. Ryu, M. Caroff, W. J. Lee, D. Mengin-Lecreulx, and B. Lemaitre. 2003. The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nat. Immunol. 4 : 478 484.
64. Lewis, L. C. 2002. Protozoan control of pests. Pp. 673 676 in P. Pimentel, ed. Encyclopedia of pest management. Marcel Dekker, New York.
65. Little, T. J., N. Colegrave, B. M. Sadd, and P. Schmid-Hempel. 2008. Studying immunity at the whole organism level. Bioessays 30 : 404 405.
66. Lohse, K., A. Gutierrez, and O. Kaltz. 2006. Experimental evolution of resistance in Paramecium caudatum against the bacterial parasite Holospora undulata. Evolution 60 : 1177 1186.
67. Luong, L. T., and M. Polak. 2007a. Costs of resistance in the Drosophila-Macrocheles system: a negative genetic correlation between ectoparasite resistance and reproduction. Evolution 61 : 1391 1402.
68. Luong, L. T., and M. Polak. 2007b. Environment-dependent trade-offs between ectoparasite resistance and larval competitive ability in the Drosophila-Macrocheles system. Heredity 99 : 632 640.
69. McKean, K. A., C. P. Yourth, B. P. Lazzaro, and A. G. Clark. 2008. The evolutionary costs of immunological maintenance and deployment. BMC Evol. Biol. 8 : 76.
70. Meister, M., and M. Lagueux. 2003. Drosophila blood cells. Cell. Microbiol. 5 : 573 580.
71. Montenegro, H., A. S. Petherwick, G. D. D. Hurst, and L. B. Klaczko. 2006. Fitness effects of Wolbachia and Spiroplasma in Drosophila melanogaster. Genetica 127 : 207 215.
72. Moret, Y., and P. Schmid-Hempel. 2000. Survival for immunity: the price of immune system activation for bumblebee workers. Science 290 : 1166 1168.
73. 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.
74. Nassonova, E. S., Y. S. Tokarev, T. Trammer, R. Entzeroth, and Y. Y. Sokolova. 2001. Phagocytosis of Nosema grylli (Microsporida, Nosematidae) spores in vivo and in vitro. J. Eukaryot. Microbiol. 48 : 83S 84S.
75. Partridge, L., and K. Fowler. 1992. Direct and correlated responses to selection on age at reproduction in Drosophila melanogaster. Evolution 46 : 76 91.
76. Perlman, S. J., and J. Jaenike. 2001. Competitive interactions and persistence of two nematode species that parasitize Drosophila recens. Ecol. Lett. 4 : 577 584.
77. Price, P. W. 1980. Evolutionary biology of parasites. Princeton Univ. Press, Princeton, NJ.
78. Refardt, D., and D. Ebert. 2007. Inference of parasite local adaptation using two different fitness components. J. Evol. Biol. 20 : 921 929.
79. Reznick, D. 1985. Costs of reproduction, an evaluation of the empirical evidence. Oikos 44 : 257 267.
80. Rigby, M. C., R. F. Hechinger, and L. Stevens. 2002. Why should parasite resistance be costly Trends Parasitol. 18 : 116 120.
81. Rivero, A., P. Agnew, S. Bedhomme, C. Sidobre, and Y. Michalakis. 2007. Resource depletion in Aedes aegypti mosquitoes infected by the microsporidia Vavraia culicis. Parasitology 134 : 1355 1362.
82. Roff, D. A. 1992. The evolution of life-histories: theory and analysis. Chapman & Hall, New York.
83. Rose, M. R. 1984. Artificial selection on a fitness component in Drosophila melanogaster. Evolution 38 : 516 526.
84. Roxstrom-Lindquist, K., O. Terenius, and I. Faye. 2004. Parasite-specific immune response in adult Drosophila melanogaster: a genomic study. Embo Rep. 5 : 207 212.
85. Sanders, A. E., C. Scarborough, S. J. Layen, A. R. Kraaijeveld, and H. C. J. Godfray. 2005. Evolutionary change in parasitoid resistance under crowded conditions in Drosophila melanogaster. Evolution 59 : 1292 1299.
86. Santos, M., K. Fowler, and L. Partridge. 1992. On the use of tester stocks to predict the competitive ability of genotypes. Heredity 69 : 489 495.
87. Sasaki, A., and H. C. J. Godfray. 1999. A model for the coevolution of resistance and virulence in coupled host-parasitoid interactions. Proc. R. Soc. Lond. B 266 : 455 463.
88. Schmid-Hempel, P. 1998. Parasites in social insects. Princeton Univ. Press, Princeton, NJ.
89. Schmid-Hempel, P., and D. Ebert. 2003. On the evolutionary ecology of specific immune defence. Trends Ecol. Evol. 18 : 27 32.
90. Schwarzenbach, G. A., and P. I. Ward. 2006. Responses to selection on phenoloxidase activity in yellow dung flies. Evolution 60 : 1612 1621.
91. Sheldon, B. C., and S. Verhulst. 1996. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11 : 317 321.
92. Stearns, S. C. 1992. The evolution of life histories. Oxford Univ. Press, Oxford.
93. Tinsley, M. C., S. Blanford, and F. M. Jiggins. 2006. Genetic variation in Drosophila melanogaster pathogen susceptibility. Parasitology 132 : 767 773.
94. Turelli, M. 1994. Evolution of incompatibility-inducing microbes and their hosts. Evolution 48 : 1500 1513.
95. Vijendravarma, R. K., A. R. Kraaijeveld, and H. C. J. Godfray. 2008. Infection of Drosophila melanogaster by Tubulinosema kingi: stage-specific susceptibility, within-host proliferation and cellular immune response. J. Invert. Path. 99 : 239 241.
96. Webster, J. P., and M. E. J. Woolhouse. 1999. Cost of resistance: relationship between reduced fertility and increased resistance in a snail-schistosome host-parasite system. Proc. R. Soc. Lond. B 266 : 391 396.
97. Weeks, A. R., M. Turelli, W. R. Harcombe, K. T. Reynolds, and A. A. Hoffmann. 2007. From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol. 5 : 997 1005.
98. Werren, J. H. 1997. Biology of Wolbachia. Annu. Rev. Entomol. 42 : 587 609.
99. Yamada, R., K. D. Floate, M. Riegler, and S. L. O'Nein. 2007. Male development time influences the strength of Wolbachia-induced cytoplasmic incompatibility expression in Drosophila melanogaster. Genetics 177 : 801 808.
100. Yan, G., D. W. Severson, and B. M. Christensen. 1997. Costs and benefits of mosquito refractoriness to malaria parasites: implications for genetic variability of mosquitoes and genetic control of malaria. Evolution 51 : 441 450.