Costs of resistance in insect-parasite and insect-parasitoid interactions

Parasitology

Volumn 125, Issue SUPPL., 2002, Pages

  Kraaijeveld, A R ^a   Ferrari, J ^a   Godfray, H C J ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Costs of resistance; Host; Immunity; Parasite; Parasitoid; Trade off

Indexed keywords

APHID; CONFERENCE PAPER; DROSOPHILA MELANOGASTER; FERTILITY; FOOD; HOST; HOST PARASITE INTERACTION; HOST RESISTANCE; INSECT; LARVA; NONHUMAN; PARASITE; PARASITOID; PEA; PLANT; POPULATION; PRIORITY JOURNAL;

ACYRTHOSIPHON PISUM; APHIDIDAE; ARACHNIDA; DROSOPHILA MELANOGASTER; HEXAPODA; INSECTA; MELANOGASTER; PISUM SATIVUM;

EID: 0036997717     PISSN: 00311820     EISSN: None     Source Type: Journal    
DOI: 10.1017/s0031182002001750     Document Type: Conference Paper

References (95)

1. ATKINSON, W. D. (1979). A field investigation of larval competition in domestic Drosophila. Journal of Animal Ecology 48, 91-102.
2. BARNES, A. I. & SIVA-JOTHY, M. T. (2000). Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor L. (Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity. Proceedings of the Royal Society London B 267, 177-182.
3. BAZZAZ, F. A., CHIARIELLO, N. R., COLEY, P. D. & PITELKA, L. F. (1987). Allocating resources to reproduction and defense. BioScience 37, 58-67.
4. BERGELSON, J. & PURRINGTON, C. B. (1996). Surveying patterns in the cost of resistance in plants. American Naturalist 148, 536-558.
5. BOOTS, M. & BEGON, M. (1993). Trade-offs with resistance to a granulosis virus in the Indian meal moth, examined by a laboratory evolution experiment. Functional Ecology 7, 528-534.
6. BOULÉTREAU, M. & WAJNBERG, E. (1986). Comparative responses of two sympatric parasitoid cynipids to the genetic and epigenetic variations of the larvae of their host, Drosophila melanogaster. Entomologia Experimentalis et Applicata 41, 107-114.
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. CARTON, Y. (1984). Analyse expérimentale de trois niveaux d'interaction entre Drosophila melanogaster et le parasite Leptopilina boulardi (sympatrie, allopatrie, xénopatrie). Génétique, Sélection, Evolution 16, 417-430.
9. CARTON, Y., BOULÉTREAU, M., VAN ALPHEN, J. J. M. & VAN LENTEREN, J. C. (1986). The Drosophila parasitic wasps. In The Genetics and Biology of Drosophila. Volume 3e (ed. Ashburner, M., Carson, L. & Thompson, J. N.), pp. 347-394. London, Academic Press.
10. CARTON, Y. & DAVID, J. R. (1983). Reduction of fitness in Drosophila adults surviving parasitization by a cynipid wasp. Experientia 39, 231-233.
11. CARTON, Y. & KITANO, H. (1979). Changes in the hemocyte population of Drosophila larvae after-single and multiple parasitization by Cothonaspis (parasitic Cynipidae). Journal of Invertebrate Pathology 34, 88-89.
12. CHAO, L., LEVIN, B. R. & STEWART, F. M. (1977). A complex community in a simple habitat: experimental study with bacteria and phage. Ecology 58, 369-378.
13. DE GREGORIO, E., SPELLMAN, P. T., RUBIN, G. M. & LEMAITRE, B. (2001). Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proceedings of the National Academy of Sciences, USA 98, 12590-12595.
14. DELPUECH, J. M., FREY, E. & CARTON, Y. (1994). Genetic and epigenetic variation in suitability of a Drosophila host to three parasitoid species. Canadian Journal of Zoology 72, 1940-1944.
15. DJAWDAN, M., CHIPPINDALE, A. K., ROSE, M. R. & BRADLEY, T. J. (1998). Metabolic reserves and evolved stress resistance in Drosophila melanogaster. Physiological Zoology 71, 584-594.
16. DOEBELI, M. (1997). Genetic variation and the persistence of predator-prey interactions in the Nicholson-Bailey model. Journal of Theoretical Biology 188, 109-120.
17. DOUMS, C. & SCHMID-HEMPEL, P. (2000). Immunocompetence in workers of a social insect, Bombus terrestris L., in relation to foraging activity and parasitic infection. Canadian Journal of Zoology 78, 1060-1066.
18. DUPAS, S., BREHÉLIN, M., FREY, D. F. & CARTON, Y. (1996). Immune suppressive virus-like particles in a Drosophila-parasitoid: significance of their intraspecific morphological variations. Parasitology 113, 207-212.
19. ESLIN, P., GIORDANENGO, P., FOURDRAIN, Y. & PRÉVOST, G. (1996). Avoidance of encapsulation in the absence of VLP by a braconid parasitoid of Drosophila larvae: an ultrastructural study. Canadian Journal of Zoology 74, 2193-2198.
20. ESLIN, P. & PRÉVOST, G. (1998). Haemocyte load and immune resistance to Asobara tabida are correlated in species of the Drosophila melanogaster subgroup. Journal of Insect Physiology 44, 807-816.
21. FELLOWES, M. D. E., KRAAIJEVELD, A. R. & GODFRAY, H. C. J. (1998a). Trade-off associated with selection for increased ability to resist parasitoid attack in Drosophila melanogaster. Proceedings of the Royal Society London B 265, 1553-1558.
22. FELLOWES, M. D. E., KRAAIJEVELD, A. R. & GODFRAY, H. C. J. (1999a). The relative fitness of Drosophila melanogaster (Diptera, Drosophilidae) that have successfully defended themselves against the parasitoid Asobara tabida (Hymenoptera, Braconidae). Journal of Evolutionary Biology 12, 123-128.
23. FELLOWES, M. D. E., KRAAIJEVELD, A. R. & GODFRAY, H. C. J. (1998b). Association between feeding rate and defence against parasitoids in Drosophila melanogaster. Evolution 53, 1302-1305.
24. FELLOWES, M. D. E., KRAAIJEVELD, A. R. & GODFRAY, H. C. J. (1999c). Cross-resistance following artificial selection for increased defence agamst parasitoids in Drosophila melanogaster. Evolution 53, 966-972.
25. FELLOWES, M. D. E., MASNATTA, P., KRAAIJEVELD, A. R. & GODFRAY, H. C. J. (1998b). Pupal parasitoid attack influences the relative fitness of Drosophila that have encapsulated larval parasitoids. Ecological Entomology 23, 281-284.
26. FELLOWES, M. D. E. & TRAVIS, J. M. J. (2000). Linking the coevolutionary and population dynamics of host-parasitoid interactions. Population Ecology 42, 195-203.
27. FERDIG, M. T., BEERNTSEN, B. T., SPRAY, F. J., LI, J. & CHRISTENSEN, B. M. (1993). Reproductive costs associated with resistance in a mosquito-filarial worm system. American Journal of Tropical Medicine and Hygiene 49, 756-762.
28. FERRARI, J., MÜLLER, C. B., KRAAIJEVELD, A. R. & GODFRAY, H. C. J. (2001). Clonal variation and covariation in aphid resistance to parasitoids and a pathogen. Evolution 55, 1805-1814.
29. FRAENKEL, G. & RUDALL, K. M. (1947). The structure of insect cuticles. Proceedings of the Royal Society London B 134, 111-143.
30. FULLILOVE, S. L., JACOBSON, A. G. & TURNER, F. R. (1977). Embryonic development: descriptive. In The Genetics and Biology of Drosophila. Volume 2c (ed. Ashburner, M. & Wright, T. R. F.), pp. 106-209. London, Academic Press.
31. GODFRAY, H. C. J. (1994). Parasitoids, Behavioral and Evolutionary Ecology. Princeton, New Jersey, Princeton University Press.
32. GREEN, D. M. (2000). Coevolutionary dynamics in a parasitoid-host system. PhD-thesis, University of London.
33. HARVEY, J. A., THOMPSON, D. J. & HEYES, T. J. (1996). Reciprocal influences and costs of parasitism on the development of Corcyra cephalonica and its endoparasitoid Venturia canescens. Entomologia Experimentalis et Applicata 81, 39-45.
34. HENTER, H. J. & VIA, S. (1995). The potential for coevolution in a host-parasitoid system. 1. Genetic variation within an aphid population in susceptibility to a parasitic wasp. Evolution 49, 427-438.
35. HERMS, D. A. & MATTSON, W. J. (1992). The dilemma of plants: to grow or defend. Quarterly Review of Biology 67, 283-335.
36. HOANG, A. (2001). Immune response to parasitism reduces resistance of Drosophila melanogaster to desiccation and starvation. Evolution 55, 2353-2358.
37. HOCHBERG, M. E. & HOLT, R. D. (1995). Refuge evolution and the population dynamics of coupled host-parasitoid associations. Evolutionary Ecology 9, 633-661.
38. HUFBAUER, R. A. (2001). Pea aphid-parasitoid interactions: have parasitoids adapted to differential resistance? Ecology 82, 717-725.
39. HUFBAUER, R. A. & VIA, S. (1999). Evolution of an aphid-parasitoid interaction: variation in resistance to parasitism among aphid populations specialized on different plants. Evolution 53, 1435-1445.
40. JOSHI, A. & MUELLER, L. D. (1988). Evolution of higher feeding rate in Drosophila due to density-dependent natural selection. Evolution 42, 1090-1093.
41. JOSHI, A. & MUELLER, L. D. (1996). Density-dependent natural selection in Drosophila: trade-offs between larval food acquisition and utilization. Evolutionary Ecology 10, 463-474.
42. KALTZ, O. & SHYKOFF, J. A. (1998). Local adaptation in host-parasite systems. Heredity 81, 361-370.
43. KÖNIG, C. & SCHMID-HEMPEL, P. (1995). Foraging activity and immunocompetence in workers of the bumble bee, Bombus terrestris L. Proceedings of the Royal Society London B 260, 225-227.
44. KRAAIJEVELD, A. R., EMMETT, D. A. & GODFRAY, H. C. J. (1997). Absence of direct sexual selection for parasitoid encapsulation in Drosophila melanogaster. Journal of Evolutionary Biology 10, 337-342.
45. KRAAIJEVELD, A. R. & GODFRAY, H. C. J. (1997). Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389, 278-280.
46. KRAAIJEVELD, A. R. & GODFRAY, H. C. J. (1999). Geographic patterns in the evolution of resistance and virulence in Drosophila and its parasitoids. American Naturalist 153, S61-S74.
47. KRAAIJEVELD, A. R. & GODFRAY, H. C. J. (2001). Is there local adaptation in Drosophila-parasitoid interactions? Evolutionary Ecology Research 3, 107-116.
48. KRAAIJEVELD, A. R., HUTCHESON, K. A., LIMENTANI, E. C. & GODFRAY, H. C. J. (2001 a). Costs of counterdefences to host resistance in a parasitoid of Drosophila. Evolution 55, 1815-1821.
49. KRAAIJEVELD, A. R., LIMENTANI, E. C. & GODFRAY, H. C. J. (2001 b). Basis of the trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Proceedings of the Royal Society London B 268, 259-261.
50. KRAAIJEVELD, A. R. & VAN ALPHEN, J. J. M. (1994). Geographical variation in resistance of the parasitoid Asobara tabida against encapsulation by Drosophila melanogaster larvae: the mechanism explored. Physiological Entomology 19, 9-14.
51. KRAAIJEVELD, A. R., VAN ALPHEN, J. J. M. & GODFRAY, H. C. J. (1998). The coevolution of host resistance and parasitoid virulence. Parasitology 116 (Suppl.), S29-S45.
52. KRAAIJEVELD, A. R. & VAN DER WEL, N. N. (1994). Geographic variation in reproductive success of the parasitoid Asobara tabida in larvae of several Drosophila species. Ecological Entomology 19, 221-229.
53. KURTZ, J., WIESNER, A., GÖTZ, P. & SAUER, K. P. (2000). Gender differences and individual variation in the immune system of the scorpionfly Panorpa vulgaris (Insecta: Mecoptera). Developmental and Comparative Immunology 24, 1-12.
54. LACKIE, A. M. (1988a). Immune mechanisms in insects. Parasitology Today 4, 98-105.
55. LACKIE, A. M. (1988b). Haemocyte behaviour. Advances in Insect Physiology 21, 85-178.
56. LENSKI, R. E. (1988). Experimental studies of pleiotropy and epistasis in Escherichia coli. I. Variation in competitive fitness among mutants resistant to virus T4. Evolution 42, 425-432.
57. LIVELY, C. M. (1999). Migration, virulence and the geographic mosaic of adaptation by parasites. American Naturalist 153, S34-S47.
58. McKEAN, K. A. & NUNNEY, L. (2001). Increased sexual activity reduces male immune function in Drosophila melanogaster. Proceedings of the National Academy of Sciences, USA 98, 7904-7909.
59. MILNER, R. J. (1982). On the occurrence of pea aphids, Acyrthosiphon pisum, resistant to isolates of the fungal pathogen Erynia neoaphidis. Entomologia Experimentalis et Applicata 32, 23-27.
60. MORET, Y. & SCHMID-HEMPEL, P. (2000). Survival for immunity: the price of immune activation for bumblebee workers. Science 290, 1166-1168.
61. MORET, Y. & SCHMID-HEMPEL, P. (2001). Immune defence in bumble-bee offspring. Nature 414, 506.
62. MÜLLER, C. B., ADRIAANSE, I. C. T., BELSHAW, R. & GODFRAY, H. C. J. (1999). The structure of an aphid-parasitoid community. Journal of Animal Ecology 68, 346-370.
63. NAPPI, A. (1975). Parasite encapsulation in insects. In Invertebrate Immunity (ed. Maramorosch, K. & Shope, R.), pp. 293-326. New York, Academic Press.
64. NAPPI, A. J., CARTON, Y. & FREY, F. (1991). Parasite-induced enhancement of hemolymph tyrosine activity in a selected immune reactive strain of Drosophila melanogaster. Archives of Insect Biochemistry and Physiology 18, 159-168.
65. NAPPI, A. & VASS, E. (1998). Hydrogen peroxide production in immune-reactive Drosophila melanogaster. Journal of Parasitology 84, 1150-1157.
66. NAPPI, A., VASS, E., FREY, F. & CARTON, Y. (1995). Superoxide anion generation in Drosophila during melanotic encapsulation of parasites. European Journal of Cell Biology 68, 450-458.
67. PENER, M. & YERUSHALMI, Y. (1998). The physiology of locust phase polymorphism: an update. Journal of Insect Physiology 44, 365-377.
68. REESON, A. F., WILSON, K., GUNN, A., HAILS, R. S. & GOULSON, D. (1998). Baculovirus resistance in the noctuid Spodoptera exempta is phenotypically plastic and responds to population density. Proceedings of the Royal Society London B 265, 1787-1791.
69. REZNICK, D. (1985). Cost of reproduction: an evaluation of the empirical evidence. Oikos 44, 257-267.
70. RIGBY, M. C. & JOKELA, J. (2000). Predator avoidance and immune defence: costs and trade-offs in snails. Proceedings of the Royal Society London B 267, 171-176.
71. RIZKI, R. M. & RIZKI, T. M. (1990). Parasitoid virus-like particles destroy Drosophila cellular immunity. Proceedings of the National Academy of Sciences, USA 87, 8388-8392.
72. RIZKI, T. M. & RIZKI, R. M. (1984). The cellular defence system of Drosophila melanogaster. In Insect Ultrastructure (ed. King, R. C. & Akai, H.), pp. 579-603. New York, Plenum Press..
73. RYDER, J. J. & SIVA-JOTHY, M. T. (2000). Male calling song provides a reliable signal of immune function in a cricket. Proceedings of the Royal Society London B 267, 1171-1175.
74. SANDSTRÖM, J. (1994). High variation in host adaptation among clones of the pea aphid, Acyrthosiphon pisum on peas, Pisum sativum. Entomologia Experimentalis et Applicata 71, 245-256.
75. SANDSTRÖM, J. & PETTERSON, J. (1994). Amino acid composition of phloem sap and the relation to interspecific variation in pea aphid (Acyrthosiphon pisum) performance. Journal of Insect Physiology 38, 93-99.
76. SASAKI, A. & GODFRAY, H. C. J. (1999). A model for the coevolution of resistance and virulence in coupled host-parasitoid interactions. Proceedings of the Royal Society London B 266, 455-463.
77. SHELDON, B. & VERHULST, S. (1996). Ecological immunity: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317-321.
78. SIVA-JOTHY, M. T. (2000). A mechanistic link between parasite resistance and expression of a sexually selected trait in a damselfly. Proceedings of the Royal Society London B 267, 2523-2527.
79. SIVA-JOTHY, M. T., TSUBAKI, Y. & HOOPER, R. E. (1998). Decreased immune response as a proximate cost of copulation and oviposition in a damselfly. Physiological Entomology 23, 274-277.
80. SIVA-JOTHY, M. T., TSUBAKI, Y., HOOPER, R. E. & PLAISTOW, S. J. (2001). Investment in immune function under chronic and acute immune challenge in an insect. Physiological Entomology 26, 1-5.
81. STARÝ, P., GONZÁLEZ, D. & HALL, J. C. (1980). Aphidius eadyi n. sp. (Hymenoptera: Aphidiidae), a widely distributed parasitoid of the pea aphid, Acyrtosiphon pisum (Harris) in the Palearctic. Entomologica Scandinavica 11, 473-480.
82. STEARNS, S. C. (1992). The Evolution of Life Histories. Oxford, Oxford University Press.
83. STRAND, M. R. & PECH, L. L. (1995). Immunological basis for compatibility in parasitoid-host relationships. Annual Review of Entomology 40, 31-56.
84. TEPASS, U., FESSLER, L. I., AZIZ, A. & HARTENSTEIN, V. (1994). Embryonic origin of hemocytes and their relationship to cell death in Drosophila. Development 120, 1829-1837.
85. TIËN, N. S. H., BOYLE, D., KRAAIJEVELD, A. R. & GODFRAY, H. C. J. (2001). Competitive ability of parasitized Drosophila larvae. Evolutionary Ecology Research 3, 747-757.
86. VERHULST, S., DIELEMAN, S. J. & PARMENTIER, H. K. (1999). A trade-off between immunocompetence and sexual ornamentation in domestic fowl. Proceedings of the National Academy of Sciences, USA 96, 4478-4481.
87. VIA, S. (1991 a). The genetic structure of host plant adaptation in a spatial patchwork - demographic variability among reciprocally transplanted: pea aphid clones. Evolution 45, 827-852.
88. VIA, S. (1991 b). Specialized host plant performance of pea aphid clones is not altered by experience. Ecology 72, 1420-1427.
89. VIA, S. (1999). Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution 53, 1446-1457.
90. VIA, S., BOUCK, A. C. & SKILLMAN, S. (2000). Reproductive isolation between divergent races of pea aphids on two hosts. II. Selection against migrants and hybrids in the parental environments. Evolution 54, 1626-1637.
91. WAJNBERG, E., BOULÉTREAU, M., PRÉVOST, G. & FOUILLET, P. (1990). Developmental relationships between Drosophila larvae and their endoparasitoid Leptopilina (Hymenoptera: Cynipidae) as affected by crowding. Archives of Insect Biochemistry and Physiology 13, 239-245.
92. WEBSTER, J. P. & WOOLHOUSE, M. E. J. (1999). Cost of resistance: relationship between reduced fertility and increased resistance in a snail-schistosome host-parasite system. Proceedings of the Royal Society London B 266, 391-396.
93. WILSON, K., COTTER, S. C., REESON, A. F. & PELL, J. K. (2001). Melanism and disease resistance in insects. Ecology Letters 4, 637-649.
94. YAN, G., SEVERSON, D. W. & CHRISTENSEN, B. M. (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.
95. ZAREH, N., WESTOBY, M. & PIMENTEL, D. (1980). Evolution in a laboratory host-parasitoid system and its effects on population kinetics. Canadian Entomologist 112, 1049-1106.