COSTS OF COUNTERDEFENSES TO HOST RESISTANCE IN A PARASITOID OF DROSOPHILA
Alex R. Kraaijeveld
Natural Environment Research Council Centre for Population Biology and Department of Biology, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, United Kingdom
E-mail: [email protected]
Search for more papers by this authorKerry A. Hutcheson
Natural Environment Research Council Centre for Population Biology and Department of Biology, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, United Kingdom
Search for more papers by this authorElizabeth C. Limentani
Natural Environment Research Council Centre for Population Biology and Department of Biology, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, United Kingdom
Search for more papers by this authorH. Charles J. Godfray
Natural Environment Research Council Centre for Population Biology and Department of Biology, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, United Kingdom
E-mail: [email protected]
Search for more papers by this authorAlex R. Kraaijeveld
Natural Environment Research Council Centre for Population Biology and Department of Biology, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, United Kingdom
E-mail: [email protected]
Search for more papers by this authorKerry A. Hutcheson
Natural Environment Research Council Centre for Population Biology and Department of Biology, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, United Kingdom
Search for more papers by this authorElizabeth C. Limentani
Natural Environment Research Council Centre for Population Biology and Department of Biology, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, United Kingdom
Search for more papers by this authorH. Charles J. Godfray
Natural Environment Research Council Centre for Population Biology and Department of Biology, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, United Kingdom
E-mail: [email protected]
Search for more papers by this authorAbstract
Abstract The ability of a parasitoid to evolve enhanced counterdefenses against host resistance and its possible costs were studied in a Drosophila-parasitoid system. We reared Asobara tabida (Braconidae, Hymenoptera) exclusively on D. melanogaster to impose artificial selection for improved counterdefenses against cellular encapsulation, the main host defense against parasitism. Controls were reared on D. subobscura, the main host of the population of wasps from which the laboratory culture was derived and a species that never encapsulates parasitoids. We observed improved survival and avoidance of encapsulation in all five selection lines compared to their paired control lines, although there was unexpected variation among pairs. Improved survival was associated with parasitoid eggs becoming embedded in host tissue, where they were protected from circulating haemocytes. There were no differences among lines in average adult size, fat content, egg load, or performance on D. subobscura. However, the duration of the egg stage in selection lines was longer than that of control lines, probably because of reduced nutrient and/or oxygen supply when eggs are embedded in host tissue. We suggest that this delay in hatching reduces the probability of parasitoid survival if another parasitoid egg is laid in the same host (superparasitism or multiparasitism) and hence is a cost of enhanced counterdefenses against host resistance.
References
- Bohannan, B. J. M., and R. E. Lenski 2000. Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol. Lett. 3: 362–377.
- Carton, Y., M. Boulètreau, J. J. M. van Alphen, and J. C. Van Lenteren 1986. The Drosophila parasitic wasps. Pp. 348–394.in J. N. Thompson, eds. The genetics and biology of Drosophila. Vol. 3e. Academic Press, London .
- 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.
- Doebeli, M. 1997. Genetic variation and the persistence of predator-prey interactions in the Nicholson-Bailey model. J. Theor. Biol. 188: 109–120.
- Driessen, G., and L. Hemerik 1992. The time and egg budget of Leptopilina clavipes, a parasitoid of larval Drosophila. Ecol. Entomol. 17: 17–27.
- 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.
- Ellers, J. 1996. Fat and eggs: an alternative method to measure the trade-off between survival and reproduction in insect parasitoids. Neth. J. Zool. 46: 227–235.
- Ellers, J., J. J. M. van Alphen, and J. G. Sevenster 1998. A field study of size-fitness relationships in the parasitoid Asobara tabida. J. Anim. Ecol. 67: 318–324.
- Eslin, P., P. Giordanengo, Y. Fourdrain, and G. Prevost 1996. Avoidance of encapsulation in the absence of VLP by a braconid parasitoid of Drosophila larvae: an ultrastructural study. Can. J. Zool. 74: 2193–2198.
- 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.
- 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.
- 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.
- Gemmill, A. W., and A. F. Read 1998. Counting the costs of disease resistance. Trends Ecol. Evol. 13: 8–9.
- Godfray, H. C. J. 1987. The evolution of clutch size in parasitic wasps. Am. Nat. 129: 221–233.
- Godfray, H. C. J. 1994. Parasitoids, behavioral and evolutionary ecology. Princeton Univ. Press, Princeton , NJ .
- Green, D. M., A. R. Kraaijeveld, and H. C. J. Godfray 2000. Evolutionary interactions between Drosophila melanogaster and its parasitoid Asobara tabida. Heredity 85: 450–458.
- Jaenike, J., and I. Dombeck 1998. General-purpose genotypes for host species utilization in a nematode parasite of Drosophila. Evolution 52: 832–840.
- Janssen, A. R. M. 1989. Optimal host selection by Drosophila parasitoids in the field. Funct. Ecol. 3: 469–479.
- Kazmer, D. J., and R. F. Luck 1995. Field tests of the size-fitness hypothesis in the egg parasitoid Trichogramma pretiosum. Ecology 76: 412–425.
- 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.
- 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.
- Kraaijeveld, A. R., E. C. Limentani, and H. C. J. Godfray 2001. Basis of the trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Proc. R. Soc. Lond. B 268: 259–261.
- Rizki, R. M., and T. M. Rizki 1990. Parasitoid virus-like particles destroy Drosophila cellular immunity. Proc. Natl. Acad. Sci. USA 87: 8388–8392.
-
Rizki, T. M., and
R. M. Rizki
1984. The cellular defence system of Drosophila melanogaster. Pp. 579–604.in
H. Akai, eds.
Insect ultrastructure. Vol. 2. Plenum Press,
New York
.
10.1007/978-1-4613-2715-8_16 Google Scholar
-
Salt, G.
1970. The cellular defence reactions of insects. Cambridge Univ. Press,
Cambridge
,
U.K.
10.1017/CBO9780511721960 Google Scholar
- 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.
- Stearns, S. C. 1992. The evolution of life histories. Oxford Univ. Press, Oxford , U.K.
-
van Strien-van Liempt, W. T. F. H.
1983. The competition between Asobara tabida Nees von Esenbeck, 1834 and Leptopilina heterotoma (Thomson, 1862) in multiparasitized hosts I..
The course of competition. Neth. J. Zool. 33: 125–163.
10.1163/002829683X00066 Google Scholar
-
van Strien-van Liempt, W. T. F. H., and
J. J. M. van Alphen
1981. The absence of interspecific host discrimination in Asobara tabida Nees and Leptopilina heterotoma (Thomson), coexisting larval parasitoids of Drosophila species.
Neth. J. Zool. 31: 701–712.
10.1163/002829681X00239 Google Scholar
- Vinson, S. B. 1990. How parasitoids deal with the immune system of their host: an overview. Arch. Ins. Biochem. Physiol 13: 3–37.
- Visser, M. E. 1994. The importance of being large: the relationship between size and fitness in females of the parasitoid Aphaereta minuta (Hymenoptera, Braconidae). J. Anim. Ecol. 63: 963–978.
- Visser, M. E., B. Luyckx, H. W. Nell, and G. J. F. Boskamp 1992. Adaptive superparasitism in solitary parasitoids: marking of parasitized hosts in relation to the pay-off from superparasitism. Ecol. Entomol. 17: 76–82.
- West, S. A., K. E. Flanagan, and H. C. J. Godfray 1996. The relationship between parasitoid size and fitness in the field, a study of Achrysocharoides zwoelferi (Hymenoptera: Eulophidae). J. Anim. Ecol. 65: 631–639.