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Physiological bases for parasite-induced alterations of host behaviour

Published online by Cambridge University Press:  16 March 2011

S. N. Thompson
Affiliation:
Department of Entomology, University of California, Riverside, California, 92521, U.S.A.
M. Kavaliers
Affiliation:
Division of Oral Biology, Faculty of Dentistry and Department of Psychology, University of Western Ontario, London, Ontario, N6A 5C1, Canada

Summary

Parasitism is defined in various ways as an intimate relationship in which one partner, the parasite, lives on or in another, the host, generally at the expense of the latter. Parasitism commonly results in a unique array of host physiological responses and adaptations. Most studies of the physiological effects of parasitism have focused on the pathological consequence of infection and disease. While many physiological changes contribute to pathogenesis, it is now recognized that parasitic infections at sub-clinical levels also produce physiological effects that either ameliorate or may not contribute to the disease process. Moreover, these physiological changes are often manifested by altered host behaviour. Behavioural studies have enabled an ecological- and evolutionary-oriented evaluation of host responses. In this fashion, physiological effects may be assessed as to whether they affect fitness and confer benefit or harm to one or both of the symbionts involved. We briefly examine how these physiological responses, specifically neural, endocrine, neuromodulatory, and immunomodulatory components, may interact to modify host behaviours. We consider the adaptiveness of these responses and how the behavioural patterns elicited may simultaneously appear adaptive for the parasite as well as the host. In addition, we address how parasite-host physiological and behavioural interactions may be altered during the course of parasitism.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1994

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References

REFERENCES

Adams, M. L., Sewing, B., Forman, J. B., Meyer, E. R. & Cicero, T. J. (1993). Opioid-induced suppression of rat testicular function. Journal of Pharmacology and Experimental Therapeutics 266, 323–28.Google ScholarPubMed
Alcock, J. (1993). Animal Behavior, Sunderland: (Sinauer Assoc).Google Scholar
Alexander, J. & Stimson, W. H. (1988). Sex hormones and the course of parasitic infection. Parasitology Today 4, 189–93.CrossRefGoogle Scholar
Alexander, J. E. Jr. & Covich, A. P. (1991). Predation risk and avoidance behavior in two freshwater snails. Biological Bulletin 180, 387–93.CrossRefGoogle ScholarPubMed
Amit, Z. & Galina, H. (1986). Stress-induced analgesia: adaptive pain suppression. Physiological Reviews 66, 1091–120.CrossRefGoogle ScholarPubMed
Anderson, R. M. & May, R. M. (1982). Coevolution of hosts and parasites. Parasitology 85, 411–26.CrossRefGoogle ScholarPubMed
Arme, C. (1968). Effects of the plerocercoid larva of a pseudophyllidean cestode, Ligula intestinalis on the pituitary gland and gonads of its host. Biological Bulletin of the Marine Biological Laboratory, Woods Hole. 134, 1525.CrossRefGoogle Scholar
Arme, C. & Owen, R. W. (1968). Occurrence and pathology of Ligula intestinalis infections in British fishes. Journal of Parasitology 54, 272–80.CrossRefGoogle ScholarPubMed
Arme, C, Griffiths, D. V. & Sumpter, J. P. (1982). Evidence against the hypothesis that the plerocercoid larva of Ligula intestinalis (Cestoda: Pseudophyllidea) produces a sex steroid that interferes with host reproduction. Journal of Parasitology 68, 169–71.CrossRefGoogle Scholar
Barlow, H. (1990). The mechanical mind. Annual Review of Neuroscience 13, 1524.CrossRefGoogle ScholarPubMed
Barnard, C. J. (1990). Parasitic relationships. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.) pp. 133. New York: Taylor & Francis.Google Scholar
Baudoin, M. (1975). Host castration as a parasitic strategy. Evolution 29, 335–52.CrossRefGoogle ScholarPubMed
Bayne, C. J. & Loker, E. S. (1987). Survival within the snail host. In The Biology of Schistosomes: from Genes to Latrines (ed. Rollinson, D. & Simpson, A. J. G.), pp. 321–46. New York: Academic Press.Google Scholar
Beckage, N. E. (1985). Endocrine interactions between endoparasitic insects and their hosts. Annual Review of Entomology 30, 371413.CrossRefGoogle Scholar
Beckage, N. E. (1993). Games that parasites play: the dynamic roles of proteins and peptides in the relationship between parasite and host. In Parasites and Pathogens of Insects (ed. Beckage, N. E.; Thompson, S. N. & Federici, B. A.) Vol.1 pp. 2557. New York: Academic Press.CrossRefGoogle Scholar
Beckage, N. E. & Riddiford, L. M. (1982). Effects of parasitism by Apanteles congregatus on the endocrine physiology of the tobacco hornworm, Manduca sexta. General and Comparative Endocrinology 47, 308–22.CrossRefGoogle ScholarPubMed
Beckage, N. E., Templeton, T., Nielsen, B. D., Cook, D. I. & Stoltz, D. B. (1987). Parasitism-induced hemolymph polypeptides in Manduca sexta (L.) larvae parasitized by the braconid wasp Cotesia congregata (Say). Insect Biochemistry 17, 439455.CrossRefGoogle Scholar
Bellinger, F. P., Madamba, S. & Siggins, G. R. (1993). Interleukin IB inhibits synaptic strength and longterm potentiation in the rat CA1 hippocampus. Brain Research 628, 227234.CrossRefGoogle Scholar
Bermudes, D. & Joiner, K. A. (1993). The role of parasites in generating evolutionary novelty. Parasitology Today 9, 458–63.CrossRefGoogle ScholarPubMed
Bethel, W. M. & Holmes, J. C. (1973). Altered evasive behavior and responses to light in amphipods harboring acanthocephalan cystacanths. Journal of Parasitology 58, 945–56.CrossRefGoogle Scholar
Bishop, R. K. & Cannon, L. R. G. (1979). Morbid behaviour of the commercial sand crab, Portunus pelagicus (L.), parasitized by Sacculina granifera Boschma, 1973 (Cirripedia: Rhizocephala). Journal of Fish Diseases 2, 131–44.CrossRefGoogle Scholar
Blanchard, D.C, Blanchard, R. J., Rodgers, R. J. & Weiss, S. M. (1990). The characterization and modeling of antipredator defensive behavior. Neuroscience and Biobehavioral Reviews 14, 463–72.CrossRefGoogle ScholarPubMed
Bodnar, R. J., Romero, M-T. & Kramer, E. (1988). Organismic variables and pain inhibition: roles of gender and aging. Brain Research Bulletin 21, 947–53.CrossRefGoogle ScholarPubMed
Brabin, L. & Brabin, B. J. (1992). Parasitic infections in women and their consequences. Advances in Parasitology 31, 181.CrossRefGoogle ScholarPubMed
Bremermann, H. J. (1987). In The Evolution of Sex and its Consequences (ed. Stearns, S. C.), pp. 135161. Basel: Birkhauser Verlag.CrossRefGoogle Scholar
Brown, J. J., Kiuchi, M., Kainoh, Y. & Takeda, S. (1993 ). In vitro release of ecdysteroids by an endoparasitoid, Ascogaster reticulatus Watanabe. Journal of Insect Physiology 39, 229–34.CrossRefGoogle Scholar
Brown, J. L. & Eklund, A. (1994). Kin recognition and the major histocompatibility complex: an integrative review. American Naturalist 143, 435–61.CrossRefGoogle Scholar
Bundy, D. A. P. (1988). Sexual effects on parasite infection. Parasitology Today 4, 186–9.CrossRefGoogle Scholar
Calcagnetti, D. J. & Holtzman, S. G. (1990). Factors affecting restraint stress-induced potentiation of morphine analgesia. Brain Research 537, 157–62.CrossRefGoogle ScholarPubMed
Camhi, J. M. (1993). Neural mechanisms of behavior. Current Opinion in Neurobiology 3, 1011–19.CrossRefGoogle ScholarPubMed
Capron, A. & Dessaint, J. P. (1989). Molecular basis of host-parasite relationship: towards the definition of protective antigens. Immunological Reviews 112, 2748.CrossRefGoogle ScholarPubMed
Cicero, T. J. (1980). Effects of exogenous and endogenous opiates on the hypothalamic-pituitarygonadal axis in the male rat. Federation Proceedings 39, 2551–4.Google Scholar
Colwell, D. D. & Kavaliers, M. (1990). Exposure to mosquitoes, Aedes togoi (Theo.) induces and augments opioid mediated analgesia in mice. Physiology and Behavior 48, 397401.CrossRefGoogle ScholarPubMed
Colwell, D. D. & Kavaliers, M. (1992). Evidence for activation of endogenous opioid systems in mice following short exposure to stable flies. Medical and Veterinary Entomology 6, 159–66.CrossRefGoogle ScholarPubMed
Colwell, D. D. & Kavaliers, M. (1993). Evidence for involvement of endogenous opioid peptides in altered nociceptive responses of mice infected with Eimeria vermiformis. Journal of Parasitology 79, 751–6.CrossRefGoogle ScholarPubMed
Coopersmith, C. B. & Lenington, S. (1992). Female preferences based on male quality in house mice: interactions between male dominance rank and tcomplex genotype. Ethology 90, 116.CrossRefGoogle Scholar
Coustau, C, Renaud, F., Delay, B., Robbins, I. & Mathieu, M. (1991). Mechanisms involved in parasitic castration: in vitro effects of the trematode Prosorhynchus squamatus on the gametogenesis and the nutrient storage metabolism of the marine bivalve mollusc Mytilus edulis. Experimental Parasitology 73, 3643.CrossRefGoogle ScholarPubMed
Crane, M. S. J. & Dvorak, J. A. (1980). Vertebrate cells express protozoan antigen after hybridization. Science 208, 194–6.CrossRefGoogle ScholarPubMed
Crook, K. (1990). Humoral and cellular effector immune responses against parasites. In Parasites: Immunity and Pathology (ed. Behnke, J. M.), pp. 89119. New York: Taylor and Francis.Google Scholar
Curtis, L. A. (1990). Parasitism and the movement of intertidal gastropod individuals. Biological Bulletin 179, 105–12.CrossRefGoogle ScholarPubMed
Dahlman, D. L. & Vinson, S. B. (1993). Teratocytes: developmental and biochemical characteristics. In Parasites and Pathogens of Insects (ed. Beckage, N. E., Thompson, S. N. & Federici, B. A.) Vol.1 pp. 145–65. New York: Academic Press.CrossRefGoogle Scholar
Damian, R. T. (1987). The exploitation of host immune responses by parasites. Journal of Parasitology 73, 313.CrossRefGoogle ScholarPubMed
Dawkins, M. S. (1990). The future of ethology: how many legs are we standing on ? Perspectives in Ethology, 8, 4754.Google Scholar
Dawkins, R. (1976). Hierarchical organization: a candidate principle for ethology. In Growing Points in Ethology (ed. Bateson, P. P. G. & Hinde, R. A.) pp. 754. Cambridge: Cambridge University Press.Google Scholar
Dawkins, R. (1982). Host phenotypes as parasite genes. In The Extended Phenotype: The Gene as the Unit of Selection, pp. 209–27. Oxford: W. H. Freeman.Google Scholar
Dawkins, R. & Krebs, J. R. (1979). Arms races between and within species. Proceedings of the Royal Society of London Series B 205, 489511.Google ScholarPubMed
de Jong-Brink, M. (1992). Interference of schistosome parasites with neuroendocrine mechanisms in their snail host causes physiological changes. Advances in Neuroimmunology 2, 199233.CrossRefGoogle Scholar
de Jong-Brink, M. & Elsaadany, M. M. (1987). Schistosomin, a parasitic factor interfering with reproduction in Lymnaea stagnalis. In Neurobiology. Molluscan Models (ed. Boer, H. H., Geraerts, W. P. M. & Joosse, J.) pp. 150–57. Amsterdam: North Holland.Google Scholar
De Jong-Brink, M., Elsaadany, M. M. & Boer, H. H. (1988). Schistosomin, an antagonist of calfluxin. Experimental Parasitology 65, 109–18.CrossRefGoogle ScholarPubMed
De Jong-Brink, M. Elsaadany, M. M. & Horadijk, P. L. (1988). Trematode parasites interfere with the endocrine control of reproduction of their intermediate hosts, freshwater snails. Tropical and Geographical Medicine 40, 276–7.Google Scholar
De Jong-Brink, M., Hordijk, P. L., Schallig, H. D. F. G., Bergamin-Sassen, M. J. M. & Oosthoek, P. (1990). Possible mechanisms underlying parasitic castration in trematode infected snails. In Advances in Invertebrate Reproduction (ed. Hoshi, M. & Yamashita, O.) Vol.5 pp. 141149. Amsterdam: Elsevier.Google Scholar
de Souza, E. B. (1993). Corticotropin-releasing factor and interleukin–1 receptors in the brain-endocrineimmune axis. Role in stress response and infection. Annals of the Nezv York Academy of Sciences 697, 927.CrossRefGoogle ScholarPubMed
Despommier, D. D. (1990). Trichinella spiralis: The worm that would be virus. Parasitology Today 6, 193–6.CrossRefGoogle ScholarPubMed
Despommier, D. D., Gold, A. M., Buck, S. W., Capo, V. & Silberstein, D. (1990). Trichinella spiralis: secreted antigen of the infective L1 larva localizes to the cytoplasm and nucleoplasm of infected host cells. Experimental Parasitology 71, 2738.CrossRefGoogle Scholar
De Jong-Brink, M., Hordijk, P. L., Schallig, H. D. F. G., Bergamin-Sassen, M. J. M. & Oosthoek, P. (1990). Possible mechanisms underlying parasitic castration in trematode infected snails. In Advances in Invertebrate Reproduction (ed. Hoshi, M. & Yamashita, O.) Vol.5 pp. 141149. Amsterdam: Elsevier.Google Scholar
Dogiel, V. A., Petrushevski, G. K. & Polyanski, Y. I. (1961). Parasitology of Fishes. Edinburgh: Oliver & Boyd.Google Scholar
Dover, B. A., Davies, D. H. & Vinson, S. B. (1988). Degeneration of last-instar Heliothis virescens prothoracic glands by Campoletis sonorensis polydnavirus. Journal of Invertebrate Pathology 51, 8091.CrossRefGoogle Scholar
Dufau, M. L., Tinajero, J. C. & Fabbri, A. (1993). Coricotropin-releasing factor: an antireproductive hormone of the testis. FASEB Journal 7, 299307.CrossRefGoogle Scholar
Duvaux-Miret, O., Leung, M. K., Capron, A. & Stefano, G. B. (1993). Schistosoma mansoni: an enkephalinergic system that may participate in internal and hostparasite signalling. Experimental Parasitology 76, 7684.CrossRefGoogle Scholar
Duvaux-Miret, O., Stefano, G. B., Smith, E. M. & Capron, A. (1992 a). Neuroimmunology of host-parasite interactions: proopiomelanocortin derived peptides in the infection by Schistosoma mansoni. Advances in Neuroimmunology 2, 297311.CrossRefGoogle Scholar
Duvaux-Miret, O., Stefano, G. B., Smith, E. M., Dissous, C. & Capron, A. (1992 b). Immunosuppression in the definitive hosts of the human parasite, Schistosoma mansoni, by release of immunoreactive neuropeptides. Proceedings of the National Academy of Sciences USA 89, 778–81.CrossRefGoogle Scholar
Egid, K. & Brown, J. L. (1989). The major histocompatability complex and female mating preferences in mice. Animal Behaviour 38, 438–50.CrossRefGoogle Scholar
Fairweather, J., Halton, D. W. & Shaw, C. (1992). Regulatory peptides in host-parasite interactions: characterization and roles in pathophysiology and immune responses. Advances in Neuroimmunology 2, 249–65.CrossRefGoogle Scholar
Federici, B. A. (1991). Viewing polydnaviruses as genetic secretions of endoparasitic Hymenoptera. Redia 74, 463–6.Google Scholar
Folstad, I. & Karter, J. (1992). Parasites, bright males, and the immunocompetence handicap. American Naturalist 139, 603–22.CrossRefGoogle Scholar
Gala, R. R. (1991). Prolactin and growth hormone in the regulation of the immune system. Proceedings of Experimental Biology and Medicine 198, 513–27.CrossRefGoogle ScholarPubMed
Garaerts, W. P. M. & Joosse, J. (1984). The reproductive biology of the Basommatophora. In The Mollusca Vol.7 Reproduction (ed. Tompa, A. S., Verdonk, N. H. & van den Biggelaar, J. A. M.), pp. 141207. New York: Academic Press.Google Scholar
Gardner, D. (1993). The Neurobiology of Neural Networks. Cambridge: MIT Press.CrossRefGoogle Scholar
Grisel, J. E., Fleshner, M., Watkins, L. R. & Maier, S. F. (1993). Opioid and nonopioid interactions in two forms of stress-induced analgesia. Pharmacology, Biochemistry and Behavior 45, 161–72.CrossRefGoogle ScholarPubMed
Grossman, C. J. (1984). Regulation of the immune system by sex steroids. Endocrine Reviews 5, 435–55.CrossRefGoogle ScholarPubMed
Grossman, C. J. (1985). Interaction between the gonadal steroids and the immune system. Science 227, 257–61.CrossRefGoogle ScholarPubMed
Grossman, C. J. (1988). The importance of hormones in the regulation of the immune system. Immunology and Allergy Practice 10, 104–12.Google Scholar
Groves, P. M. & Schlesinger, K. (1982). Biological Psychology. Dubuque: William C. Brown.Google Scholar
Hamilton, W. D. (1980). Sex versus non-sex versus parasite. Oikos 35, 282–90.CrossRefGoogle Scholar
Hamilton, W. D. & Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384–7.CrossRefGoogle Scholar
Hamilton, W. D., Axelrod, R. E. & Tanese, R. (1990). Sexual reproduction as an adaptation to resist parasites (a review). Proceedings of the National Academy of Sciences USA 87, 3566–73.CrossRefGoogle ScholarPubMed
Harris-Warrick, R. M., Flamm, R. E., Johnson, B. R. & Katz, P. S. (1989). Modulation of neural circuits in crustacea. American Zoologist 29, 1305–20.CrossRefGoogle Scholar
Harris-Warrick, R. M. & Marder, E. (1991). Modulation of neural networks for behavior. Annual Review of Neuroscience 14, 3957.CrossRefGoogle Scholar
Haseeb, M. A. & Fried, B. (1988). Chemical communication in helminths. Advances in Parasitology 27, 170207.Google ScholarPubMed
Haufe, W. O. (1988) Host-parasite interactions of bloodfeeding dipterans in health and productivity of mammals. International Journal for Parasitology 17, 607–14.CrossRefGoogle Scholar
Heale, R. V., Vanderwolf, C. H. & Kavaliers, M. (1994). Components of weasel and fox odors elicit fast wave bursts in the dentate gyrus of rats. Behavioural Brain Research (in press).CrossRefGoogle Scholar
Heiligenberg, W. (1991). The neural basis of behavior: a neuroethological view. Annual Review of Neuroscience 14, 247–67.CrossRefGoogle ScholarPubMed
Helluy, S. & Holmes, J. C. (1990). Serotonin, octopamine, and the clinging behavior induced by the parasite Polymorphus paradoxus (Acanthocephala) in Gammarus lacustris (Crustacea). Canadian Journal of Zoology 68, 1214–20.CrossRefGoogle Scholar
Herz, A. (1993). Opioids I & II, Springer-Verlag, New York.CrossRefGoogle Scholar
Hinde, R. A. (1990). The interdependence of the behavioural sciences. Transactions of the Royal Society of London B329, 217–27.Google ScholarPubMed
Holmes, J. C. & Bethel, W. M. (1972). Modification of intermediate host behaviour by parasites. In Behavioural Aspects of Parasite Transmission (eds. Canning, E. U. & Wright, C. A.) pp. 123149. London: Academic Press.Google Scholar
Holmes, J. C. & Zohar, S. (1990). Pathology and host behaviour. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.) pp. 3463. New York: Taylor & Francis.Google Scholar
Hordijk, P. L. (1991). Structure of the snail neuropeptide schistosomin and its role in the hostparasite interaction: Lymnaea stagnalis - Trichobilharzia ocellata. Thesis. Free University. Amsterdam.Google Scholar
Horton, D. R. & Moore, J. (1993). Behavioral effects of parasites and pathogens in insect hosts. In Parasites and Pathogens of Insects (ed. Beckage, N. E., Thompson, S. N. & Federici, B. A.) Vol.1 pp. 107–24. New York: Academic Press.CrossRefGoogle Scholar
Howard, R. S. & Lively, C. M. (1994). Parasitism, mutation accumulation and the maintenance of sex. Nature 367, 554–5.CrossRefGoogle ScholarPubMed
Howell, M. J. (1981). An approach to the production of helminth antigens in vitro: the formation of hybrid cells between Fasciola hepatica and a rat fibroblast cell line. International Journal for Parasitology 11, 235–42.CrossRefGoogle Scholar
Huntingford, F. (1984). The Study of Animal Behaviour. New York: Chapman and Hall.CrossRefGoogle Scholar
Hurd, H. (1990a). Physiological and behavioural interactions between parasites and invertebrate hosts. Advances in Parasitology 29, 272318.Google ScholarPubMed
Hurd, H. (1990b). Parasite induced modulation of insect reproduction. In Advances in Invertebrate Reproduction (ed. Hoshi, M. & Yamashita, O.) Vol.5 pp. 163169. Amsterdam: Elsevier.Google Scholar
Hurd, H. (1993). Reproductive disturbances induced by parasites and pathogens of insects. In Parasites and Pathogens of Insects (ed. Beckage, N. E., Thompson, S. N. & Federici, B. A.) Vol.1 pp. 87105. New York: Academic Press.CrossRefGoogle Scholar
Hurd, H. & Arme, C. (1986a). Hymenolepis diminuta: The effect of metacestodes upon egg production and viability in the intermediate host, Tenebrio molitor. Journal of Invertebrate Pathology 47, 225–31.CrossRefGoogle ScholarPubMed
Hurd, H. & Arme, C. (1986 b). Hymenolepis diminuta: Influence of metacestodes upon synthesis and secretion of fat body protein and its ovarian sequestration in the intermediate host, Tenebrio molitor. Parasitology 93, 111–20.CrossRefGoogle ScholarPubMed
Hurd, H. & Arme, C. (1987a). Hymenolepis diminuta (Cestoda): the role of intermediate host sex in the establishment, growth and development of metacestodes in Tenebrio molitor (Coleoptera). Helminthologia 24, 2331.Google Scholar
Hurd, H. & Arme, C. (1987b). Hymenolepis diminuta: Effect of infection upon the patency of the follicular epithelium of the intermediate host Tenebrio molitor. Journal of Invertebrate Pathology 49, 227–34.CrossRefGoogle ScholarPubMed
Hurd, H. & Parry, G. (1991). Metacestode-induced depression of the production of, and response to, sex pheromone in the intermediate host Tenebrio molitor. Journal of Invertebrate Pathology 58, 82–7.CrossRefGoogle ScholarPubMed
Hurd, H., Strambi, C. & Beckage, N. E. (1990). Hymenolepis diminuta: An investigation of juvenile hormone titre, degradation and supplementation in the intermediate host, Tenebrio molitor. Parasitology 100, 445–2.CrossRefGoogle ScholarPubMed
Hurd, H. & Weaver, R. J. (1987). Evidence against the hypothesis that metacestodes of Hymenolepis diminuta inhibit corpora allata functioning in the intermediate host, Tenebrio molitor. Parasitology 95, 93–7.CrossRefGoogle ScholarPubMed
Immelmann, K. & Beer, C. (1989). A Dictionary of Ethology. Cambridge: Harvard University Press.Google Scholar
Irie, Y. & Iwamura, Y. (1993). Host-related Dna sequences are localized in the body of schistosome adults. Parasitology 107, 519–28.CrossRefGoogle ScholarPubMed
Isseroff, H., Sylvester, P. W., Bessette, C. L., Jones, P. L., Fisher, W. G., Rynkowski, T. & Gregor, K. T. (1989). Schistosomiasis: role of endogenous opioids in suppression of gonadal steroid secretion. Comparative Biochemistry and Physiology 94A, 41–5.CrossRefGoogle ScholarPubMed
Isseroff, H., Sylvester, P. W. & Held, W. A. (1986). Effects of Schistosoma mansoni on androgen regulated gene expression in the mouse. Molecular and Biochemical Parasitology 18, 401–12.CrossRefGoogle ScholarPubMed
Iwamura, Y., Irie, Y. Kominama, R., Nara, T. & Yasuraoka, K. (1991). Existence of host-related Dna sequences in the schistosome genome. Parasitology 102, 397403.CrossRefGoogle ScholarPubMed
Joosse, J. (1988). The hormones of molluscs. In Invertebrate Endocrinology, Vol.3, Endocrinology of Selected Invertebrate Types, (eds. Laufer, H. & Downer, G. H.) pp. 89140. New York: Alan R. Liss.Google Scholar
Joosse, J. & Van Elk, R. (1983). Intervention of a trematode parasite in the action of the female gonadotrophic hormones on the albumen gland of Lymnaea stagnalis. In Molluscan Neuroendocrinology (eds. Lever, J. & Boer, H. H.) pp. 118–20. Amsterdam: North Holland.Google Scholar
Joosse, J. & Van Elk, R. (1986). Trichobilharzia ocellata: Physiological characterization of giant growth, glycogen depletion, and absence of reproductive activity in the intermediate snail host, Lymnaea stagnalis. Experimental Parasitology 62, 113.CrossRefGoogle ScholarPubMed
Joosse, J., Van Elk, R., Mosselman, S., Wortelboer, H. & Van Diepen, J. C. E. (1988). Schistosomin: a pronasesensitive agent in the hemolymph of Trichobilharzia ocellata-infected Lymnaea stagnalis inhibits the activity of albumen glands in vitro. Parasitology Research 74, 228–34.CrossRefGoogle ScholarPubMed
Kabata, Z. (1981). Copepoda (Crustacea) parasitic on fishes: problems and perspectives. Advances in Parasitology 19, 171.Google Scholar
Kalat, J. W. (1984). Biological Psychology. Belmont: Wadsworth.Google Scholar
Kavaliers, M. (1988). Evolutionary and comparative aspects of nociception. Brain Research Bulletin 21, 923–31.CrossRefGoogle ScholarPubMed
Kavaliers, M. (1992). Opioid systems, behavioral thermoregulation and shell polymorphism in the land snail Cepaea nemoralis. Journal of Comparative Physiology B162, 172–8.CrossRefGoogle Scholar
Kavaliers, M. & Colwell, D. D. (1991). Sex differences in opioid and nonopioid mediated predator-induced analgesia in mice. Brain Research 568, 173–7.CrossRefGoogle ScholarPubMed
Kavaliers, M. & Colwell, D. D. (1992a). Parasitism, opioid systems and host behaviour. Advances in Neuroimmunology 2, 287–92.CrossRefGoogle Scholar
Kavaliers, M. & Colwell, D. D. (1992b). Exposure to the scent of male mice infected with the protozoan parasite, Eimeria vermiformis, induces opioid and nonopioid-mediated analgesia in female mice. Physiology and Behavior 52, 373–7.CrossRefGoogle Scholar
Kavaliers, M. & Colwell, D. D. (1993a). Multiple opioid system involvement in the mediation of parasiticinfection induced analgesia. Brain Research 623, 316–20.CrossRefGoogle ScholarPubMed
Kavaliers, M. & Colwell, D. D. (1993b). Aversive responses of female mice to the odors of parasitized males: neuromodulatory mechanisms and implications for mate choice. Ethology 95, 202–12.CrossRefGoogle Scholar
Kavaliers, M. & Colwell, D. D. (1994). Parasite infection attenuates nonopioid mediated predator-induced analgesia in mice. Physiology and Behavior 55, 505–10.CrossRefGoogle ScholarPubMed
Kavaliers, M. & Colwell, D. D. & Galea, L. A. M. (1993). Spatial learning impairment in parasitized mice. Society for Neuroscience Abstracts 19, 365.Google Scholar
Kavaliers, M. & Innes, D. G. L. (1987). Stress-induced opioid analgesia and activity in deer mice: sex and population differences. Brain Research 425, 4956.CrossRefGoogle ScholarPubMed
Kavaliers, M. & Podesta, R. B. (1988). Opioid involvement in parasite-induced behavioural modifications: evidence from hamsters infected with Schistosoma mansoni. Canadian Journal of Zoology 66, 2653–7.CrossRefGoogle Scholar
Kavaliers, M., Podesta, R. B., Hirst, M. & Young, B. (1984). Evidence for activation of the endogenous opiate system in hamsters infected with human blood flukes, Schistosoma mansoni. Life Sciences 35, 2365–73.CrossRefGoogle ScholarPubMed
Kennedy, J. S. (1993). The New Anthropomorphism. New York: Cambridge University Press.Google Scholar
Kirchgessner, A. L., Bodnar, R. J. & Pasternak, G. W. (1987). Naloxazone and pain-inhibitory systems: evidence for a collateral inhibition model. Pharmacology, Biochemistry and Behavior 17, 1175–9CrossRefGoogle Scholar
Ko, R. C., Fan, L. & Lee, D. L. (1992). Experimental reorganization of host muscle cells by excretory/secretory products of infective Trichinella spiralis larvae. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 77–8.CrossRefGoogle ScholarPubMed
KO, R. C., Fan, L., Lee, D. L. & Compton, H. (1994). Changes in host muscles induced by excretory/secretory products of larval Trichinella spiralis and Trichinella pseudospiralis. Parasitology 108, 195205.CrossRefGoogle ScholarPubMed
Krebs, J. R. & Horn, G. (1993). Behavioural and Neural Aspects of Learning and Memory. Oxford: Claredon Press.Google Scholar
Kvalsvig, J. D. (1988). The effect of parasitic infection on cognitive performance. Parasitology Today 41, 206–8.CrossRefGoogle Scholar
Lafferty, K. D. (1992). Foraging on prey that are modified by parasites. American Naturalist 140, 854–67.CrossRefGoogle Scholar
Lawrence, P. O. (1990). The biochemical and physiological effects of insect hosts on the development and ecology of their insect parasites: An overview. Archives of Insect Biochemistry and Physiology 13, 217–28.CrossRefGoogle Scholar
Lawrence, P. O. (1991). Hormonal effects on insects and other endoparasites in vitro. In Vitro Cellular and Developmental Biology 27A, 487–96.CrossRefGoogle Scholar
Lawrence, P. O. & Lanzrein, B. (1993). Hormonal interactions between insect endoparasites and their host insects. In Parasites and Pathogens of Insects (ed. Beckage, N. E., Thompson, S. N. & Federici, B. A.) Vol.1 pp. 5986. New York: Academic Press.CrossRefGoogle Scholar
Lefcort, H. & Bayne, C. J. (1991). Thermal preferences of resistant and susceptible strains of Biomphalaria glabrata (Gastropoda) exposed to Schistosoma mansoni (Trematoda). Parasitology 103, 357–62.CrossRefGoogle ScholarPubMed
Lewis, J. W., Cannon, J. T. & Liebeskind, J. C. (1980). Opioid and non-opioid mechanisms of stress analgesia. Science 208, 623–5.CrossRefGoogle Scholar
Lightowlers, M. W. & Rickard, M. D. (1988). Excretorysecretory products of helminth parasites: effects on host immune responses. Parasitology 96, S12366.CrossRefGoogle ScholarPubMed
Lively, C. M. (1987). Evidence from a New Zealand snail for the maintenance of sex by parasitism. Nature 328, 519–21.CrossRefGoogle Scholar
Maier, S. F., Wiertelak, E. P., Martin, D. & Watkins, L. R. (1993). Interleukin-1 mediates the behavioral hyperalgesia produced by lithium chloride and endotoxin. Brain Research 623, 321–4.CrossRefGoogle ScholarPubMed
Mankau, S. K. (1977). Sex as a factor of infection of Tribolium spp. by Hymenolepis diminuta. Environmental Entomology 6, 233–6.CrossRefGoogle Scholar
Marr, D. (1982). Vision. New York: Freeman.Google Scholar
Maynard Smith., J. (1985). Sexual selection, handicaps and true fitness. Journal of Theoretical Biology 115, 18.CrossRefGoogle Scholar
Mcclelland, G. & Bourns, T. K. R. (1969). Effects of Trichobilharzia ocellata on growth, reproduction and survival of Lymnaea stagnalis. Experimental Parasitology 24, 137–46.CrossRefGoogle ScholarPubMed
McFarland, D. J. & Houston, A. (1981). Quantitative Ethology. London: Pitman.Google Scholar
McGaugh, J. L., Introini-Collison, I. B. & Castellano, C. (1993). Involvement of opioid peptides in learning and memory. In: Opioids II (ed. Herz, A.). New York: Springer-Verlag, pp. 429–48.CrossRefGoogle Scholar
Milinski, M. (1990). Parasites and host decision-making. In: Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.). pp. 95116 London: Taylor & Francis.Google Scholar
Millar, D. B., Thomas, J. R., Pacheco, N. D. & Rollwagen, F. M. (1993). Natural killer cell cytoxicity and T-cell proliferation is enhanced by avoidance behavior. Brain Behavior and Immunity 7, 144–53.CrossRefGoogle Scholar
Minchella, D. J. (1985). Host life-history variation in response to parasitism. Parasitology 90, 205–16.CrossRefGoogle Scholar
Moller, A. P., Dufva, R, & Allander, K. (1993). Parasites and the evolution of host social behaviour. Advances in the Study of Behaviour 22, 65101.CrossRefGoogle Scholar
Moore, J. & Gotelli, N. J. (1990). A phylogenetic perspective on the evolution of altered host behaviours: a critical look at the manipulation hypothesis. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.) pp. 193233. New York: Tavlor and Francis.Google Scholar
Morris, R. G. M. (1984). Development of a water-maze procedure for studying spatial learning in the rat. Journal of Neuroscience Methods 11, 4760.CrossRefGoogle ScholarPubMed
Moser, M. & Taylor, S. (1978). Effects of the copepod Cardiodectes medusaeus on the laternfish Stenobrachius leucopsarus with notes on hypercastration by the hydroid Hydrichythys sp. Canadian Journal of Zoology 56, 2372–6.CrossRefGoogle Scholar
Mueller, J. F. (1980). A growth factor produced by a larval tapeworm and its biological activity. In Growth and Growth Factors (ed. Shizume, K. & Takano, K.) pp. 193201. Baltimore: University Park Press.Google Scholar
Nee, S. (1988). The password effect of sex in fungi. Trends in Ecology and Evolution 3, 218–19.CrossRefGoogle Scholar
Nelson, W. A. (1989). Metabolic responses of livestock to hematophagous arthropod invasion. In: Physiological Interactions Between Hematophagous Arthropods and their Vertebrate Hosts. Entomological Society of America. Miscellaneous Publication 71 (ed. Jones, C. J. & Williams, R. E.) pp. 1521.Google Scholar
Nokes, C. & Bundy, D. A. P. (1994). Does helmith infection affect mental processing and educational achievement. Parasitology Today 19, 1418.CrossRefGoogle Scholar
Oitzel, M. S., Van Oers, H., Schobitz, B. & De Kloet, E. R. (1993). Interleukin 1B, but not interleukin–6, impairs spatial navigation learning. Brain Research 613, 160–3.CrossRefGoogle Scholar
Pearson, E. J. & Cheng, T. C. (1985). Studies on parasitic castration: occurrence of a gametogenesis-inhibiting factor in extract of Zoogonus lasis (Trematoda). Journal of Invertebrate Pathology 46, 239–46.CrossRefGoogle Scholar
Phares, C. K. (1992). Biological characteristics of the growth hormone-like factor from pleroceroids of the tapeworm Spirometra mansonoides. Advances in Neuroimmunology 2, 235–47.CrossRefGoogle Scholar
Phares, C. K. & Booth, B. J. M. (1987). Antihuman growth hormone antibodies cross-react with the growth hormone-like factor from plerocercoids of the tapeworm, Spirometra mansonoides. Endocrinology 121, 1839–44.CrossRefGoogle Scholar
Phares, C. K. & Cox, G. S. (1987). Molecular hybridization and immunological data support the hypothesis that the tapeworm, Spirometra mansonoides has acquired a human growth hormone gene. In Molecular Paradigms for Eradicating Helminthic Parasites (ed. Maclnnis, A. J.) pp. 391405. New York: Alan R. Liss.Google Scholar
Phares, C. K. & Watts, D. J. (1988). The growth hormone-like factor produced by tapeworm Spirometra mansonoides specifically binds receptors of cultured human lymphocytes. Journal of Parasitology 74, 896–8.CrossRefGoogle ScholarPubMed
Pomiankowski, A. N. (1987). The costs of choice in sexual selection. Journal of Theoretical Biology 128, 195218.CrossRefGoogle ScholarPubMed
Pomiankowski, A. N. (1988). The evolution of female mate preference for male genetic quality. Oxford Surveys in Evolutionary Biology 5, 136184.Google Scholar
Potts, W. K. & Wakeland, E. K. (1990). Evolution and diversity at the Major Histocompatability Complex. Trends in Ecology and Evolution 5, 181–4.CrossRefGoogle Scholar
Potts, W. K., Manning, C. J. & Wakeland, E. K. (1991). Mating patterns in semi-natural populations of mice influenced by Mhc genotype. Nature 352, 619–21.CrossRefGoogle Scholar
Read, A. F. (1990). Parasites and the evolution of host sexual behaviour. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.) pp. 117–57. New- York: Taylor & Francis.Google Scholar
Reeve, H. K. & Sherman, P. W. (1993). Adaptation and the goals of evolutionary research. Quarterly Review of Biology 68, 132.CrossRefGoogle Scholar
Rodgers, R. J. & Cooper, S. J. (1988). Endorphins, Opiates and Behavioural Processes. New York: Wiley.Google Scholar
Schallig, H. D. F. H., Hordijk, P. L., Oosthoek, P. W. & De Jong-Brink, M. (1991 b). Schistosomin, a peptide present in the haemolymph of Lymnaea stagnalis infected with Trichobilharzia ocellata, is produced only in the snail's central nervous system. Parasitology Research 77, 152–6.CrossRefGoogle Scholar
Schallig, H. D. F. H., Sassen, M. J. M., Hordijk, P. L. & DE Jong-Brink, M. (1991 a). Trichobilharzia ocellata: influence of infection on the fecundity of its intermediate snail host Lymnaea stagnalis and cercarial induction of the release of schistosomin, a snail neuropeptide antagonizing female gonadotropic hormones. Parasitology 102, 8591.CrossRefGoogle ScholarPubMed
Schmidt, O. & Schuchmann-Feddersen, I. (1989). Role of virus-like particles in parasitoid-host interaction of insects. In Subcellular Biochemistry (ed. Harris, J. R.) Vol.15 pp. 91119. New York: Plenum.Google Scholar
Schom, C., Novak, M. & Evans, W. S. (1981). Evolutionary implications of Tribolium confusum - Hymenolepis citelli interactions. Parasitology 83, 7790.CrossRefGoogle ScholarPubMed
Schopf, A. (1984). Endokrinologische untersuchungen an dem wirt-parasit-system: Pieris brassicae – Apanteles glomeratus. Entomologia Experimentalis et Applicata 36, 265–72.CrossRefGoogle Scholar
Schrag, S. J. & Rollinson, D. (1994). Effects of Schistosoma haematobium infection on reproductive success and male outcrossing ability in the simultaneous hermaphrodite, Bulinus truncatus (Gastropoda: Planorbidae). Parasitology 108, 2734.CrossRefGoogle Scholar
Schrag, S. J. & Read, A. F. (1992). Temperature determination of male outcrossing ability in a simultaneous hermaphrodite gastropod. Evolution 46, 1698–707.CrossRefGoogle Scholar
Sei, Y., Arora, P. K., Skilnick, P. & Paul, I. A. (1992). Spatial learning impairment in a murine model of AIDS. FASEB Journal 6, 3008–13.CrossRefGoogle Scholar
Sharp, S. E., Phares, C. K. & Heidrick, M. L. (1982). Immunological aspects associated with suppression of hormone levels in rats infected with plerocercoids of Spirometra mansonoides (Cestoda). Journal of Parasitology 68, 993–8.CrossRefGoogle ScholarPubMed
Sherry, D. F., Jacobs, L. F. & Gaulin, J. C. (1992). Spatial memory and adaptive specialization of the hippocampus. Trends in Neuroscience 15, 298303.CrossRefGoogle ScholarPubMed
Sluiters, J. F. (1981). Development of Trichobilharzia ocellata in Lymnaea stagnalis and the effects of infection of the reproductive system of the host. Zeitschrift für Parasitenkunde 64, 303–19.CrossRefGoogle ScholarPubMed
Sluiters, J. F. (1988). Parasite-host relationship of the avian schistosome Trichobilharzia ocellata and the hermaphrodite gastropod Lymnaea stagnalis. Thesis. Free University. Amsterdam.Google Scholar
Sluiters, J. F., Brussaard-Wust, C. C. M. & Meuleman, E. A. (1980). The relationship between miracidial dose, production of cercaria and reproductive activity of the host in the combination Trichobilharzia ocellata and Lymnaea stagnalis. Zeitschrift fur Parasitenkunde 63, 1326.CrossRefGoogle ScholarPubMed
Soldevila, A. I. & Jones, D. (1993). Expression of a parasitism-specific protein in lepidopteran hosts of Chelonus sp. Archives of Insect Biochemistry and Physiology 24, 149–69.CrossRefGoogle ScholarPubMed
Soldevila, A. I. & Jones, D. (1994). Characterization of a novel protein associated with the parasitization of lepidopteran hosts by an endoparasitic wasp. Insect Biochemistry and Molecular Biology 24, 2938.CrossRefGoogle ScholarPubMed
Solomon, G. B. (1969). Host hormones and parasitic infection. International Review of Tropical Medicine 3, 101–58.Google ScholarPubMed
Spindler, K.-D. (1988). Parasites and hormones In Parasitology in Focus (ed. Mehlhorn, H.) pp. 465–76.New York: Springer-Verlag.CrossRefGoogle Scholar
Sprent, J. F. A. (1969). Evolutionary aspects of immunity in zooparasitic infections. In Immunity to Parasitic Animals (ed. Jackson, G. J., Herman, R. & Singer, I.), pp. 362.Amsterdam: North Holland.Google Scholar
Steelman, S. L., Morgan, E. R., Cuccaro, A. J. & Glitzer, M. S. (1970). Growth hormone-like activity in hypophysectomized rats implanted with Spirometra mansonoides spargana. Proceedings of the Society of Experimental Biology and Medicine 133, 269–73.CrossRefGoogle Scholar
Stefano, G. B. (1989). Role of opioid neuropeptides in immunoregulation. Progress in Neurobiology 33, 149–59.CrossRefGoogle ScholarPubMed
Stefano, G. B., Smith, E. R. & Hughes, T. K. (1991). Opioid induction of immunoreactive interleukin-1 in Mytilus edulis and human immunocytes: an interleukin-1-like substance in invertebrate neural tissue. Journal of Neuroimmunology 32, 2934.CrossRefGoogle ScholarPubMed
Stibbs, H. H. (1984). Neurochemical and activity changes in rats infected with Trypanosoma brucei gambiense. Journal of Parasitology 70, 428–32.CrossRefGoogle ScholarPubMed
Stibbs, H. H. & Curtis, D. A. (1987). Neurochemical changes in experimental African trypanosomiasis in voles and mice. Annals of Tropical Medicine and Parasitology 81, 673–79.CrossRefGoogle ScholarPubMed
Stoltz, D. B. (1993). The polydnavirus life cycle. In Parasites and Pathogens of Insects (ed. Beckage, N. E.; Thompson, S. N. & Federici, B. A.) Vol.1 pp. 167–87.New York: Academic Press.CrossRefGoogle Scholar
Stoltz, D. B., Krell, P., Summers, M. D. & Vinson, S. B. (1984). Polydnaviridae- a proposed family of insect viruses with segmented, double-stranded, circular Dna genomes. Intervirology 21, 14.CrossRefGoogle ScholarPubMed
Stoltz, D. B., Krell, P. J. & Vinson, S. B. (1981). Polydisperse viral DNA's in ichneumonid ovaries: a survey. Canadian Journal of Microscopy 21, 123–30.CrossRefGoogle Scholar
Stoltz, D. B. & Vinson, S. B. (1979). Viruses and parasitism in insects. Advances in Virology Research 24, 125–71.CrossRefGoogle ScholarPubMed
Strand, M. R., Dover, B. A. & Johnson, J. A. (1990). Alterations in the ecdysteroid and juvenile hormone esterase profiles of Trichoplusia ni parasitized by the polyembryonic wasp Copidosoma floridanum. Archives of Insect Biochemistry and Physiology 13, 4151.CrossRefGoogle Scholar
Strand, M. R., Goodman, W. G. & Baehrecke, E. H. (1991). The juvenile hormone titer of Trichoplusia ni and its potential role in embryogenesis of the polyembryonic wasp Copidosoma floridanum. Insect Biochemistry 21, 530–33.CrossRefGoogle Scholar
Sullivan, J. T., Cheng, T. C. & Howland, K. H. (1985). Studies on parasitic castration: castration of Ilyanassa obsoleta (Mollusca: Gastropoda) by several marine trematodes. Transactions of the American Microscopical Society 104, 154–71.CrossRefGoogle Scholar
Taub, D. D., Eisenstein, E. B., Geller, B., Adler, M. & Rodgers, T. J. (1991). Immunomodulatory activity of µ- and K-selective opioid agonists. Proceedings of the National Academy of Sciences Usa 88, 360–4.CrossRefGoogle Scholar
Terman, G. W., Shavit, Y., Lewis, J. W., Cannon, J. T. & Liebeskind, J. C. (1984). Intrinsic mechanisms of pain inhibition: activation by stress. Science 226, 1270–7.CrossRefGoogle ScholarPubMed
Teskey, G. C. & Kavaliers, M. (1988). Effects of opiate agonists and antagonists on aggressive encounters and subsequent opioid- induced analgesia, activity and feeding responses in male mice. Pharmacology, Biochemistry and Behavior 31, 4352.CrossRefGoogle ScholarPubMed
Theron, A. & Gerard, C. (1994). Development of accessory sexual organs in Biomphalaria glabrata (Planorbidae) in relation to timing of infection by Schistosoma mansoni: consequences for energy utilization patterns by the parasite. Journal of Molluscan Studies 60, 2531.CrossRefGoogle Scholar
Theron, A., Gerard, C. & Moneie, H. (1992). Early enhanced growth of the digestive gland of Biomphalaria glabrata infected with Schistosoma mansoni: side effect or parasite manipulation? Parasitology Research 78, 445–50.CrossRefGoogle ScholarPubMed
Thompson, S. N. (1983). Biochemical and physiological effects of metazoan endoparasites on their host species. Comparative Biochemistry and Physiology 74B, 183211.Google ScholarPubMed
Thompson, s. N. (1985). Metabolic integration during the host associations of multicellular animal endoparasites. Comparative Biochemistry and Physiology 81B, 2142.Google ScholarPubMed
Thompson, S. N. (1990). Physiological alterations during parasitism and their effects on host behaviour. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.) pp. 6494.New York: Taylor & Francis.Google Scholar
Tinbergen, N. (1954). Some neurophysiological problems raised by ethology. British Journal of Animal Behaviour 2, 115.CrossRefGoogle Scholar
Tinbergen, N. (1963). On aims and methods of ethology. Zeitschrift fur Tierpsychologie 20, 410–33.CrossRefGoogle Scholar
Vanderwolf, C. H. (1988). Cerebral activity and behavior: control by central cholinergic and serotonergic systems. International Review of Neurobiology 30, 225340.CrossRefGoogle ScholarPubMed
Wakelin, D. (1976). Host responses. In Ecological Aspects of Parasitology (ed. Kennedy, C. R.), pp. 115–41.Amsterdam: North-Holland.Google Scholar
Watkins, L. R., Wiertelak, E. P., Goehler, L. E., Mooney-Heiberger, K., Martinez, J., Furness, L., Smith, K. P. & Maier, S. F. (1994). Neurocircuitry of illness-induced hyperalgesia. Brain Research 639, 283–99.CrossRefGoogle ScholarPubMed
Whitfield, J. B. (1990). Parasitoids, polydnaviruses and endosymbiosis. Parasitology Today 6, 381–4.CrossRefGoogle ScholarPubMed
Wilson, R. A. (1993). Immunity and immunoregulation in helmith infections. Current Opinion in Immunology 5, 538–7.CrossRefGoogle Scholar
Wright, C. A. (1969). The pathogenesis of helminths in Mollusca. Helminthological Abstracts 35, 207–24.Google Scholar
Wülker, W. (1975). Parasite-induced castration and intersexuality in insects. In Inter sexuality in theAnimal Kingdom (ed. Reinboth, R.) pp. 121–34. Berlin: Springer.Google Scholar
Zuk, M. (1990). Reproductive strategies and disease susceptibility: an evolutionary viewpoint. Parasitology Today 6, 231–33.CrossRefGoogle ScholarPubMed
Zuk, M. (1992). The role of parasites in sexual selection: current evidence and future directions. Advances in the Study of Bhavior 21, 3968.CrossRefGoogle Scholar