Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-19T12:47:11.493Z Has data issue: false hasContentIssue false
  • English
  • Français

The coevolution of host resistance and parasitoid virulence

Published online by Cambridge University Press:  16 March 2011

A. R. Kraaijeveld ,
J. J. M. Van Alphen  and
H. C. J. Godfray
A. R. Kraaijeveld
Affiliation:
Department of Biology and NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, UK.
J. J. M. Van Alphen
Affiliation:
Institute of Evolutionary and Ecological Sciences, University of Leiden, Kaiserstraat 63, PO Box 9516, 2300 RA Leiden, The Netherlands.
H. C. J. Godfray
Affiliation:
Department of Biology and NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, UK.
Get access Rights & Permissions [Opens in a new window]

Summary

Host-parasitoid interactions are abundant in nature and offer great scope for the study of coevolution. A particularly fertile area is the interaction between internal feeding parasitoids and their hosts. Hosts have evolved a variety of means of combating parasitoids, in particular cellular encapsulation, while parasitoids have evolved a wide range of countermeasures. Studies of the evolution of host resistance and parasitoid virulence are reviewed, with an emphasis on work involving Drosophila and its parasitoids. Genetic variation in both traits has been demonstrated using isofemale line and artificial selection techniques. Recent studies have investigated the fitness costs of maintaining the ability to resist parasitoids, the comparative fitness of flies that have successfully defended themselves against parasitoids, and the degree to which resistance and virulence act against one or more species of host or parasitoid. A number of studies have examined geographical patterns, and sought to look for local adaptation; or have compared the traits across a range of species. Finally, the physiological and genetic basis of change in resistance and virulence is being investigated. While concentrating on Drosophila, the limited amount of work on different systems is reviewed, and other possible areas of coevolution in host-parasitoid interactions are briefly discussed.

Keywords

ResistancevirulencehostparasitoidgeneticsDrosophila
Type
Research Article
Information
Parasitology , Volume 116 , supplement S1: Symposia of the British Society for Parasitology Volume 35: Parasite-insect interactions: reciprocal manipulation , 1998 , pp. S29 - S45
Copyright
Copyright © Cambridge University Press 1998

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Asgari, S. & Schmidt, O. (1994). Passive protection of eggs from the parasitoid, Cotesia rubecula, in the host, Pieris rapae. Journal of Insect Physiology 40, 789–795.CrossRefGoogle Scholar
Askew, R. R. & Shaw, M. R. (1986). Parasitoid communities: their size, structure and development. In Insect Parasitoids(ed. Waage, J. K. & Greathead, D.), London, Academic Press.Google Scholar
Beckage, N. E., Thompson, S. N. & Federici, B. A. (1993). Parasites and Pathogens of Insects. Volume 1: Parasites. San Diego, Academic Press.Google Scholar
Benassi, V., Frey, F. & Carton, Y. (1998). A new specific gene for wasp cellular immune resistance in Drosophila Heredity (in press).CrossRefGoogle Scholar
Boulétreau, M. (1986). The genetic and coevolutionary interactions between parasitoids and their hosts. In Insect Parasitoids(ed. Waage, J. K. & Greathead, D.), pp. 169–200. London, Academic Press.Google Scholar
Boulétreau, M. & Fouillet, P. (1982). Variablitié génétique intrapopulation de l'adéquation de Drosophila melanogaster à un de ses parasites hyménoptères. Comptes rendu de l'Académie des Sciences 295, 775–778.Google 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
Brehélin, M. (1986). Immunity in Invertebrates. Berlin, Springer Verlag.CrossRefGoogle Scholar
Carton, Y. (1984). Analyse expérimentale de trois niveaux d'interactions entre Drosophila melanogaster et le parasite Leptopilina boulardi (sympatrie, allopatrie, xénopatrie). Genetics, Selection & Evolution 16, 417–430.CrossRefGoogle Scholar
Carton, Y. (1987). Ecological and genetic significance of the encapsulation process in Drosophila against a parasitic wasp. Les Collogues de l'INRA 58, 99–100.Google Scholar
CARTON, Y. & Boulétreau, M. (1985). Encapsulation ability of Drosophila melanogaster: a genetic analysis. Developmental & Comparative Immunology 9, 211–219.CrossRefGoogle Scholar
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.Google Scholar
Carton, Y., Cary, P. & Nappi, A. (1989). Genetic variability of host-parasite relationship traits: utilization of isofemale lines in a Drosophils simulans parasitic wasp. Genetics, Selection & Evolution 21, 437–446.CrossRefGoogle Scholar
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. & David, J. R. (1985). Relation between the genetic variability of digging behaviour of Drosophila larvae and their susceptibility to a parasitic wasp. Behavioural Genetics 15, 403–408.CrossRefGoogle Scholar
Carton, Y., Frey, F. & Nappi, A. (1992). Genetic determinism of the cellular immune reaction in Drosophila melanogaster. Heredity 69, 393–399.CrossRefGoogle Scholar
Carton, Y. & Kitano, H. (1981). Evolutionary relationships to parasitism by seven species of the Drosophila melanogaster subgroup. Biological Journal of the Linnean Society 16, 227–241.CrossRefGoogle Scholar
Carton, Y. & Nappi, A. (1992). Methods for genetic investigation of cellular immune reaction in insects, with the parasitic {Drosophila) system as a model. In Insect Immunity(ed. Pathak, J. P. N.), pp. 91–101. Oxford, Oxford & IBH Publishing Company.Google Scholar
Carton, Y. & Nappi, A. (1997). Drosophila cellular immunity against parasitoids. Parasitology Today 13, 217–227.CrossRefGoogle Scholar
Carton, Y. & Nappi, A. J. (1991). The Drosophila immune reaction and the parasitoid capacity to evade it: genetic and coevolutionary aspects. Acta Oecologica 12, 89–104.Google Scholar
Carton, Y. & Sokolowski, M. B. (1992). Interactions between searching strategies of Drosophila parasitoids and the polymorphic behaviour of their hosts. Journal of Insect Behaviour 5, 161–175.CrossRefGoogle Scholar
Carton, Y. & Sokolowski, M. B. (1994). Parasitization of embedded and non-embedded Drosophila melanogaster (Diptera: Drosophilidae) pupae by the parasitoid Pachycrepoideus vindemniae (Hymenoptera: Pteromalidae). Journal of Insect Behaviour 7, 129–131.CrossRefGoogle Scholar
Cousteau, C., Rocheleau, T., Carton, Y., Nappi, A. J. & Ffrench Constant, R. H. (1996). Induction of a putative serine protease transcript in immune challenged Drosophila. Developmental & Comparative Immunology 20, 265–272.CrossRefGoogle Scholar
De Belle, J. S., Hilliker, A. J. & Sokolowski, M. B. (1989). Genetic localization of foraging (for), a major gene for larval behaviour in Drosophila melanogaster. Genetics 123, 157–163.Google Scholar
De Belle, J. S. & Sokolowski, M. B. (1987). Heredity of rover/sitter: alternative foraging strategies of Drosophila melanogaster larvae. Journal of Heredity 75, 131–134.Google Scholar
De Belle, J. S., Sokolowski, M. B. & Hilliker, A. J. (1993). Genetic analysis of the foraging microregion of Drosophila melanogaster. Genome 36, 94–101.Google 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
Dicke, M. (1998). Evolution of induced indirect defense of plants. In Evolution of Induced Defenses(ed. Harvell, C. D. & Tollrien, R.). Princeton, Princeton University Press (in press).Google Scholar
Dicke, M. & Sabelis, M. W. (1988). Infochemical terminology: based on cost-benefit analysis rather than origin of compounds. Functional Ecology 2, 131–139.CrossRefGoogle Scholar
Driessen, G., Hemerik, L. & Boonstra, B. (1991). Host selection behaviour in relation to survival in hosts of Leptopilina clavipes, a parasitoid of larval Drosophila. Netherlands Journal of Zoology 41, 99–111.CrossRefGoogle 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
Dupas, S., Frey, D. F. & Carton, Y. (1998). A single parasitoid segregating factor controls immune suppression in Drosophila. Journal of Heredity (in press).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. (1996). Variation in Drosophila concentration of haemocytes associated with different ability to encapsulate Asobara tabida larval parasitoid. Journal of Insect Physiology 42, 549–555.CrossRefGoogle Scholar
Eslin, P. & Prévost, G. (1998). Hemocyte load and immune resistance to Asobara tabida are correlated in species of the Drosophila melanogaster subgroup. Journal of Insect Physiology (in press).CrossRefGoogle Scholar
Falconer, D. S. (1996). Introduction to Quantitative Genetics (third edition). London, Longman Group UK Ltd.Google Scholar
Fellowes, M. D. E., Kraaijeveld, A. R. & Godfray, H. C. J. (1999). The relative fitness of Drosophila melanogaster (Diptera, Drosophilidae) after successful defence against the parasitoid Asobara tabida (Hymenoptera, Braconidae). Journal of Evolutionary Biology (in press).CrossRefGoogle Scholar
Fellowes, M. D., Masnatta, E. P., Kraaijeveld, A. R. & Godfray, H. C. J. (1998). Pupal parasitoid attack influences the relative fitness of Drosophila that have encapsulated larval parasitoids. Ecological Entomology (in press).CrossRefGoogle Scholar
Fleming, J.-A. G. W. (1992). Polydnaviruses: mutualists and pathogens. Annual Review of Entomology 37, 401–425.CrossRefGoogle ScholarPubMed
Gillespie, J., Kanost, M. R. & Trenczek, T. (1997). Biological mediators of insect immunity. Annual Review of Entomology 42, 611–643.CrossRefGoogle ScholarPubMed
Godfray, H. C. J. (1994). Parasitoids, Behavioral and Evolutionary Ecology. Princeton, New Jersey, Princeton University Press.CrossRefGoogle Scholar
Godfray, H. C. J. & Hassell, M. P. (1991). Encapsulation and host-parasitoid population dynamics. In Parasite-Host Association: Coexistence or Conflict(ed. Toft, C. A., Aeschlimann, A. & Bolis, L.), pp. 131–147. Oxford, Oxford University Press.CrossRefGoogle Scholar
Godfray, H. C. J. & Müller, C. B. (1998). Host-parasitoid dynamics. In Insect Population Dynamics(ed. Dempster, J. P. & Maclean, I.). London, Academic Press (in press).Google Scholar
Hadorn, E. & Grassman, A. (1962). Drosophila und Pseudeucolia IV. Artspezifsche Unterschiede in der Abwehrreaktion auf verschieden resistente Wespenstämme. Schweizerische Gesellschaft für Verberbungs-forschung Jahresbericht. 37, 21–27.Google Scholar
Hadorn, E. & Walker, I. (1960). Drosophila und Pseudeucolia. I Selektionsversuche zur Steigerung der Abwehrreaktion des Wirtes gegen den Parasiten. Revue Suisse de Zoologie 67, 216225.CrossRefGoogle Scholar
Hamilton, W. D. & Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387.CrossRefGoogle Scholar
Hassell, M. P. (1978). The Dynamics of Arthropod Predator-Prey Systems. Princeton, Princeton University Press.Google ScholarPubMed
Hassell, M. p. (1998). The Dynamics of Insect-Parasitoid Interactions. Oxford, Oxford University Press.Google Scholar
Henter, H. J. (1995). The potential for coevolution in a host-parasitoid system. 2. Genetic variation within a population of wasps in the ability to parasitize an aphid host. Evolution 49, 439–445.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
Hoffmann, A. A. & Parsons, P. A. (1988). The analysis of quantitative variation in natural populations with isofemale strains. Genetics, Selection and Evolution 20, 87–98.CrossRefGoogle Scholar
Hughes, K. & Sokolowski, M. B. (1996). Natural selection in the laboratory for a change in resistance by Drosophila melanogaster to the parasitoid wasp Asobara tabida. Journal of Insect Behaviour 9, 477–491.CrossRefGoogle Scholar
Ives, W. G. H. & Muldrew, J. A. (1981). Pristiphora erichsonii (Hartig), Larch Sawfly (Hymenoptera: Tenthredinidae). In Biological Control Programmes Against Insects and Weeds in Canada 1960–1980 (ed. Kelleher, J. S. & Hulme, M. A.), pp. 369–380. Slough, UK, Commonwealth Agricultural Bureau.Google Scholar
Janssen, A. (1989). Optimal host selection by Drosophila parasitoids in the field. Functional Ecology 3, 469–479.CrossRefGoogle Scholar
King, B. H. (1987). Offspring sex ratios in parasitoid wasps. Quarterly Review of Biology 62, 367–396.CrossRefGoogle Scholar
Kraaijeveld, A. R. (1994). Local Adaptations in a Parasitoid-host System. PhD thesis: University of Leiden.Google 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.Google 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.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. (1995). Geographical variation in encapsulation ability of Drosophila melanogaster larvae and evidence for parasitoid-specific components. Evolutionary Ecology 9, 10–17.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
Lackie, A. M. (1988). Immune mechanisms in insects. Parasitology Today 4, 98–105.CrossRefGoogle Scholar
Lawton, J. H. (1986). The effects of parasitoids on phytophagous insect communities. In Insect Parasitoids (ed. Waage, J. K. & Greathead, D.), pp. 265–287. London, Academic Press.Google Scholar
Lewis, W. J. & Tumlinson, J. H. (1988). Host detection by chemically mediated associative learning in a parasitic wasp. Nature 331, 257–259.CrossRefGoogle Scholar
Micha, S. G., Stammel, J. & Höller, C. (1993). 6- Methyl-5-heptene-2-one, a putative sex and spacing pheromone of the aphid hyperparasitoid, Alloxysta victrix (Hymenoptera: Alloxystidae). European Journal of Entomology 90, 439–442.Google Scholar
Mills, N. J. & Getz, W. M. (1996). Modelling the biological control of insect pests: a review of host-parasitoid models. Ecological Modelling 92, 121–143.CrossRefGoogle Scholar
Monconduit, H. & Prévost, G. (1994). Avoidance of encapsulation by Asobara tabida, a larval parasitoid of Drosophila species. Norwegian Journal of Agricultural Sciences Supplement 16, 301–310.Google Scholar
Muldrew, J. A. (1953). The natural immunity of the larch sawfly (Pristophora erichsonii Htg.) to the introduced parasite Mesoleius tenthredinis Morley in Manitoba and Saskatchewan. Canadian Journal of Zoology 31, 313–332.CrossRefGoogle Scholar
Murdoch, W. W. & Briggs, C. J. (1996). Theory for biological control: recent developments. Ecology 77, 2001–2013.CrossRefGoogle Scholar
Myers, J. H. (1981). Interactions between western tent caterpillars and wild rose - a test of some general plant herbivore hypotheses. Journal of Animal Ecology 50, 11–25.CrossRefGoogle Scholar
Nappi, A. (1981). Cellular immune response of Drosophila melanogaster against Asobara tabida. Parasitology 83, 319–324.CrossRefGoogle Scholar
Nappi, A., Carton, Y. & Frey, F. (1991). Parasite induced enhancement of haemolymph tyrosinase 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., 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
Nordlander, G. (1980). A revision of the genus Leptopilina Förster, with notes on the status of some other genera (Hymenoptera, Cynipidae, Eucoilidae). Entomologica Scandinavica 11, 428–453.CrossRefGoogle Scholar
Nordlund, D. A., Jones, R. L. & Lewis, W. J. (1981). Semiochemicals, their Role in Pest Control. New York, John Wiley.Google Scholar
Oprecht, E. & Hadorn, E. (1952). Stock-specific defence reactions against a parasite. Drosophila Information Service 26, 116.Google Scholar
Orr, H. A. & Irving, S. (1997). The genetics of adaption: the genetic basis of resistance to wasp parasitism in Drosophila melanogster. Evolution 51, 1877–1885.Google Scholar
Osborne, K. A., Robichon, A., Burgess, E., Butland, S., Shaw, R. A., Coulthard, A., Pereira, H. S., Greenspan, R. J. & Sokolowski, M. B. (1997). Natural behavior polymorphism due to cGMP-dependent protein kinase of Drosophila. Science 111,834–836.Google Scholar
Parsons, P. A. (1980). Isofemale strains and evolutionary strategies in natural populations. In Evolutionary Biology (ed. Hecht, M., Steere, W. & Wallace, B.), New York, Plentum Publishing Corporation.Google Scholar
Pimentel, D. (1968). Population regulation and genetic feedback. Science 159, 1432–1437.CrossRefGoogle ScholarPubMed
Pimentel, D., Levin, S. A. & Olson, D. A. (1978). Coevolution and the stability of exploiter-victim systems. American Naturalist 112, 119–125.CrossRefGoogle Scholar
Pimentel, D., Nagel, M. P. & Madden, J. L. (1963). Space-time structure of the environment and the survival of parasite-host systems. American Naturalist 97, 141–167.CrossRefGoogle Scholar
Ratcliffe, N. (1993). Cellular defence responses of insects: unresolved problems. In Parasities and Pathogens of Insects, Volume I. Parasites, (ed. Beckage, N., Thompson, S. N. & Federici, B. A.), pp. 267–304. San Diego, Academic Press.CrossRefGoogle Scholar
Read, D. P., Feeny, P. P. & Root, R. B. (1970). Habitat selection by the aphid parasite Diaeretiella rapae and its hyperparasitoid, Charips brassicae. Canadian Entomologist 102, 1567–1578.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, Volume 2 (ed. King, P. C. & Akai, H.), pp. 579–604. New York, Plenum Press.CrossRefGoogle Scholar
Riski, T. M. & Riski, R. M. (1994). Parasitoid-induced cellular immune deficiency in Drosophila. Annals of the New York Academy of Science 712, 178–194.CrossRefGoogle Scholar
Russo, J., Dupas, S., Frey, F., Carton, Y. & Brehélin, M. (1996). Insect immunity: early events in the encapsulation process of parasitoid (Leptopilina boulardi) eggs in resistant and susceptible strains of Drosophila. Parasitology 112, 135–142.CrossRefGoogle Scholar
Salt, G. (1970). The Cellular Defence Reactions of Insects. Cambridge, Cambridge University Press.CrossRefGoogle Scholar
Salt, G. & Van Den Bosch, R. (1967). The defence reactions of three species of Hypera (Coleoptera: Curculionidae) to an ichneumon wasp. Journal of Invertebrate Pathology 9, 164–177.CrossRefGoogle Scholar
Schlegel-Oprecht, E. (1953). Versuche zur Auslösung von Mutationen bei der zoophaen Cynipide Pseudeucoila bochei Weld und Befunde über die stammspezifische Abwekrreaktion des Wirtes Drosophila melanogaster. Zeitschrift für Induktive Abstammungs-und Verberbungslehre 85, 245–281.Google Scholar
Schmidt, O. & Schuchman-Feddersen, I. (1989). Role of virus-like particles in parasitoid-host interactions of insects. Subcellular Biochemistry 15, 91–119.CrossRefGoogle Scholar
Sokolowski, M. B. (1980). Foraging strategies of Drosophila melanogaster: a chromosomal analysis. Behavioural Genetics 10, 291–302.CrossRefGoogle Scholar
Sokolowski, M. B., Bauer, S. J., Wai Ping, V., Rodriguez, L., Wong, J. L. & Kent, C. (1986). Ecological genetics and behaviour of Drosophila melanogaster larvae in nature. Animal Behaviour 34, 403–408.CrossRefGoogle Scholar
Sokolowski, M. B. & Turlings, T. C. J. (1987). Drosophila parasitoid-host interactions: vibrotaxis and ovipositor searching from the host's perspectives. Canadian Journal of Zoology 65, 461–464.CrossRefGoogle Scholar
Strand, M. R. & Pech, L. L. (1995). Immunological basis for compatibility in parasitoid-host relationships. Annual Review of Entomology 40, 31–56.CrossRefGoogle Scholar
Thompson, J. N. (1982). Interaction and Coevolution. New York, John Wiley.CrossRefGoogle Scholar
Thompson, J. N. (1986). Oviposition behaviour and searching efficiency in a natural population of a braconid parasitoid. Journal of Animal Ecology 55, 351–360.CrossRefGoogle Scholar
Turlings, T. C. J. & Tumlinson, J. H. (1992). Systemic release of chemical signals by herbivore-injured corn. Proceedings of the National Academy of Sciences, USA 89, 8399–8402.CrossRefGoogle Scholar
Van Alphen, J. J. M. & Janssen, A. R. M. (1982). Host selection by Asobara tabida Nees (Braconidae: Alysiinae), a larval parasitoid of fruit inhabiting Drosophila species. II. Host species selection. Netherlands Journal of Zoology 32, 215–231.Google Scholar
Van Alphen, J. J. M. & Jervis, M. (1995). Foraging behaviour. In The Study of Natural Enemies, (ed. Jervis, M. & Kidd, N. K.), pp. 1–62. London, Chapman & Hall.Google Scholar
Van Alphen, J. J. M. & Thunnissen, I. (1983). Host selection and sex allocation by Pachcrepoides vindemiae Rondani (Pteromalidae) as a facultative hyperparasitoid of Asobara tabida Nees (Braconidae: Alysiinae) and Leptopilina heterotoma (Cynipoidea: Eucoilidae). Netherlands Journal of Zoology 32, 232–260.CrossRefGoogle Scholar
Van Alphen, J. J. M. & Vet, L. E. M. (1986). An evolutionary approach to host finding and selection. In Insect Parasitoids (ed. Waage, J. K. & Greathead, D.), pp. 23–61. London, Academic Press.Google Scholar
Van Alphen, J. J. M. & VISSER, M. E. (1990). Superparasitism as an adaptive strategy for insect parasitoids. Annual Review of Entomology 35, 59–79.CrossRefGoogle ScholarPubMed
Van Den Bosch, R. (1964). Encapsulation of the eggs of Bathyplectes curculiionis (Thompson) (Hymenoptera: Ichneumonidae) in larvae of Hypera brunneipennis (Boheman) and Hypera postica (Gyllenhal) (Coleoptera: Curculionidae). Journal of Invertebrate Pathology 6, 343–367.Google Scholar
Vass, E., Nappi, A. & Carton, Y. (1993). Comparative study of immune competence and host susceptibility in Drosophila melanogaster parasitised by Leptopilina boulardi and Asobara tabida. Journal of Parasitology 79, 106–112.CrossRefGoogle Scholar
Vet, L. E. M. & Van Alphen, J. J. M. (1985). A comparative function approach to the host detection behaviour of parasitic wasps. I. A qualitative study on Eucoilidae and Alysiinae. Oikos 44, 478–486.CrossRefGoogle Scholar
Vinson, S. B. (1997). The behaviour of parasitoids. In Comprehensive Insect Physiology, Biochemistry & Pharmacology (ed. Kerkut, G. A. & Gilbert, L. I.), pp. 417–469. New York, Pergamon Press.Google Scholar
Vinson, S. B. & Iwantsch, G. F. (1980). Host suitability for insect parasitoids. Annual Review of Entomology 25, 397–419.CrossRefGoogle Scholar
Waage, J. K. (1986). Family planning in parasitoids. In Insect Parasitoids (ed. Waage, J. K. & Greathead, D.), pp. 63–95. London, Academic Press.Google Scholar
Wajnberg, E., Prévost, G. & Boulétreau, M. (1985). Genetic and epigenetic variation in Drosophila larvae suitability to a hymenopterous endoparasitoid. Entomophaga 30, 187–192.CrossRefGoogle Scholar
Walker, I. (1959). Die Abwehrreaktion des Wirtes Drosophila melanogaster gegen die zoophage Cynipidae Pseudeucolia bochei Weld. Revue Suisse de Zoologie 66, 569–632.Google Scholar
Walker, I. (1961). Drosophila und Pseudeucolia. II. Schwierigkeiten beim Nachweis eines Selektionserfolges. Revue Suisse de Zoologie 68, 252–263.CrossRefGoogle Scholar
Walker, I. (1962). Drosophila und Pseudeucolia. III. Selektionsversucke zur Steigerung der Resistenz des Parasiten gegen die Abwehrreaktion des Wirtes. Revue Suisse de Zoologie 69, 209–227.CrossRefGoogle Scholar
Weis, A. E. (1996). Variable selection on Eurosta's gall size. 3. Can an evolutionary response to selection be detected? Journal of Evolutionary Biology 9, 623–640.CrossRefGoogle Scholar
Weis, A. E. & Abrahamson, W. G. (1985). Potential selective pressures by parasitoids on a plant–herbivore interaction. Ecology 66, 1261–1269.CrossRefGoogle Scholar
Weis, A. E., Abrahamson, W. G. & Andersen, M. C. (1992). Variable selection on Eurosta's gall size. I. The extent and nature of variation in phenotypic selection. Evolution 46, 1674–1697.Google Scholar
Weis, A. E., Abrahamson, W. G. & Mccrea, K. D. (1985). Host gall size and oviposition success by the parasitoid Eurytoma gigantea. Ecological Entomology 10, 341–348.CrossRefGoogle Scholar
Weis, A. E. & Kapelinski, A. (1994). Variable selection on Eurosta's gall size. 2. A path analysis of the ecological factors behind selection Evolution 48, 734–745.Google Scholar
Weis, A. E., Mccrea, K. D. & Abrahamson, W. G. (1989). Can there be an escalating arms race without cooevolution? Implications from a host-parasitoid simulation. Evolutionary Ecology 3, 361–370.CrossRefGoogle Scholar
Wong, J. L., Sokolowski, M. B. & Kent, C. (1985). Prepupation behaviour in Drosophila: embedding. Behavior Genetics 15, 155–165.CrossRefGoogle Scholar
Zareh, N., Westoby, M. & Pimentel, D. (1980). Evolution in a laboratory host-parasitoid system and its effect on population kinetics. Canadian Entomologist 112, 1049–1060.CrossRefGoogle Scholar
Zuk, M., Simmons, L. W. & Rotenberry, J. T. (1995). Acoustically-orienting parasitoids in calling and silent males of the field cricket Teleogryllus oceanicus. Ecological Entomology 20, 380–383.CrossRefGoogle Scholar