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

Published online by Cambridge University Press:  29 May 2003

A. R. KRAAIJEVELD ,
J. FERRARI  and
H. C. J. GODFRAY
A. R. KRAAIJEVELD
Affiliation:
NERC Centre for Population Biology and Department of Biological Sciences, Imperial College at Silwood Park, Ascot, Berks, SL5 7PY, UK
J. FERRARI
Affiliation:
NERC Centre for Population Biology and Department of Biological Sciences, Imperial College at Silwood Park, Ascot, Berks, SL5 7PY, UK
H. C. J. GODFRAY
Affiliation:
NERC Centre for Population Biology and Department of Biological Sciences, Imperial College at Silwood Park, Ascot, Berks, SL5 7PY, UK
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Abstract

Most, if not all, organisms face attack by natural enemies and will be selected to evolve some form of defence. Resistance may have costs as well as its obvious benefits. These costs may be associated with actual defence or with the maintenance of the defensive machinery irrespective of whether a challenge occurs. In this paper, the evidence for costs of resistance in insect-parasite and insect-parasitoid systems is reviewed, with emphasis on two host-parasitoid systems, based on Drosophila melanogaster and pea aphids as hosts. Data from true insect-parasite systems mainly concern the costs of actual defence; evidence for the costs of standing defences is mostly circumstantial. In pea aphids, the costs of standing defences have so far proved elusive. Resistance amongst clones is not correlated with life-time fecundity, whether measured on good or poor quality plants. Successful defence by a D. melanogaster larva results in a reduction in adult size and fecundity and an increased susceptibility to pupal parasitoids. Costs of standing defences are a reduction in larval competitive ability though these costs only become important when food is limited. It is concluded that costs of resistance can play a pivotal role in the evolutionary and population dynamic interactions between hosts and their parasites.

Keywords

Costs of resistancehostimmunityparasiteparasitoidtrade-off
Type
Research Article
Information
Parasitology , Volume 125 , Issue 7 , May 2002 , pp. S71 - S82
Copyright
© 2002 Cambridge University Press

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References

ATKINSON, W. D. (1979). A field investigation of larval competition in domestic Drosophila. Journal of Animal Ecology 48, 91–102.CrossRefGoogle Scholar
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.Google Scholar
BAZZAZ, F. A., CHIARIELLO, N. R., COLEY, P. D. & PITELKA, L. F. (1987). Allocating resources to reproduction and defense. BioScience 37, 58–67.CrossRefGoogle Scholar
BERGELSON, J. & PURRINGTON, C. B. (1996). Surveying patterns in the cost of resistance in plants. American Naturalist 148, 536–558.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
CARTON, Y., BOULÉTREAU, M., VAN ALPHEN, J. J. M. & VANLENTEREN, 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.
CARTON, Y. & DAVID, J. R. (1983). Reduction of fitness in Drosophila adults surviving parasitization by a cynipid wasp. Experientia 39, 231–233.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
DOEBELI, M. (1997). Genetic variation and the persistence of predator-prey interactions in the Nicholson-Bailey model. Journal of Theoretical Biology 188, 109–120.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
FELLOWES, M. D. E., KRAAIJEVELD, A. R. & GODFRAY, H. C. J. (1999c). Cross-resistance following artificial selection for increased defence against parasitoids in Drosophila melanogaster. Evolution 53, 966–972.Google Scholar
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.Google Scholar
FELLOWES, M. D. E. & TRAVIS, J. M. J. (2000). Linking the coevolutionary and population dynamics of host-parasitoid interactions. Population Ecology 42, 195–203.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
FRAENKEL, G. & RUDALL, K. M. (1947). The structure of insect cuticles. Proceedings of the Royal Society London B 134, 111–143.CrossRefGoogle Scholar
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.
GODFRAY, H. C. J. (1994). Parasitoids, Behavioral and Evolutionary Ecology. Princeton, New Jersey, Princeton University Press.
GREEN, D. M. (2000). Coevolutionary dynamics in a parasitoid-host system. University of London
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.CrossRefGoogle Scholar
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.Google Scholar
HERMS, D. A. & MATTSON, W. J. (1992). The dilemma of plants: to grow or defend. Quarterly Review of Biology 67, 283–335.CrossRefGoogle Scholar
HOANG, A. (2001). Immune response to parasitism reduces resistance of Drosophila melanogaster to desiccation and starvation. Evolution 55, 2353–2358.CrossRefGoogle Scholar
HOCHBERG, M. E. & HOLT, R. D. (1995). Refuge evolution and the population dynamics of coupled host-parasitoid associations. Evolutionary Ecology 9, 633–661.CrossRefGoogle Scholar
HUFBAUER, R. A. (2001). Pea aphid-parasitoid interactions: have parasitoids adapted to differential resistance? Ecology 82, 717–725.Google Scholar
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.CrossRefGoogle Scholar
JOSHI, A. & MUELLER, L. D. (1988). Evolution of higher feeding rate in Drosophila due to density-dependent natural selection. Evolution 42, 1090–1093.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
KALTZ, O. & SHYKOFF, J. A. (1998). Local adaptation in host-parasite systems. Heredity 81, 361–370.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
KRAAIJEVELD, A. R. & GODFRAY, H. C. J. (1997). Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389, 278–280.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
KRAAIJEVELD, A. R. & GODFRAY, H. C. J. (2001). Is there local adaptation in Drosophila-parasitoid interactions? Evolutionary Ecology Research 3, 107–116.Google Scholar
KRAAIJEVELD, A. R., HUTCHESON, K. A., LIMENTANI, E. C. & GODFRAY, H. C. J. (2001a). Costs of counterdefences to host resistance in a parasitoid of Drosophila. Evolution 55, 1815–1821.Google Scholar
KRAAIJEVELD, A. R., LIMENTANI, E. C. & GODFRAY, H. C. J. (2001b). 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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
LACKIE, A. M. (1988a). Immune mechanisms in insects. Parasitology Today 4, 98–105.Google Scholar
LACKIE, A. M. (1988b). Haemocyte behaviour. Advances in Insect Physiology 21, 85–178.Google Scholar
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.Google Scholar
LIVELY, C. M. (1999). Migration, virulence and the geographic mosaic of adaptation by parasites. American Naturalist 153, S34–S47.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
MORET, Y. & SCHMID-HEMPEL, P. (2000). Survival for immunity: the price of immune activation for bumblebee workers. Science 290, 1166–1168.CrossRefGoogle Scholar
MORET, Y. & SCHMID-HEMPEL, P. (2001). Immune defence in bumble-bee offspring. Nature 414, 506.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
NAPPI, A. (1975). Parasite encapsulation in insects. In Invertebrate Immunity (ed. MARAMOROSCH, K. & SHOPE, R.), pp. 293–326. New York, Academic Press.CrossRef
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.CrossRefGoogle Scholar
NAPPI, A. & VASS, E. (1998). Hydrogen peroxide production in immune-reactive Drosophila melanogaster. Journal of Parasitology 84, 1150–1157.CrossRefGoogle Scholar
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.Google Scholar
PENER, M. & YERUSHALMI, Y. (1998). The physiology of locust phase polymorphism: an update. Journal of Insect Physiology 44, 365–377.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
REZNICK, D. (1985). Cost of reproduction: an evaluation of the empirical evidence. Oikos 44, 257–267.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRef
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
SHELDON, B. & VERHULST, S. (1996). Ecological immunity: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317–321.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
STEARNS, S. C. (1992). The Evolution of Life Histories. Oxford, Oxford University Press.
STRAND, M. R. & PECH, L. L. (1995). Immunological basis for compatibility in parasitoid-host relationships. Annual Review of Entomology 40, 31–56.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
VIA, S. (1991a). The genetic structure of host plant adaptation in a spatial patchwork – demographic variability among reciprocally transplanted pea aphid clones. Evolution 45, 827–852.Google Scholar
VIA, S. (1991b). Specialized host plant performance of pea aphid clones is not altered by experience. Ecology 72, 1420–1427.Google Scholar
VIA, S. (1999). Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution 53, 1446–1457.Google Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
WILSON, K., COTTER, S. C., REESON, A. F. & PELL, J. K. (2001). Melanism and disease resistance in insects. Ecology Letters 4, 637–649.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar