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Host life-history variation in response to parasitism

  • D. J. Minchella (a1)

Over half of all living species of plants and animals are parasitic, which by definition involves intimate association with and unfavourable impact on hosts (Price, 1980). This paper will only consider parasites whose ‘unfavourable impact’ adversely affects the birth and/or mortality rates of their hosts (Anderson, 1978). Most organisms are potential hosts and must deal with the problem of parasitism. The probability of parasitic infection of a host is influenced by both environmental and genetic factors. Traditionally it was assumed that a host was either resistant or susceptible to a particular parasite and therefore the interaction between a parasite and potential host had only two possible outcomes: either the resistant host rebuffed the parasitic attack and remained uninfected or the parasite successfully invaded and significantly reduced the reproductive success of the susceptible host. This approach, however, ignored the intraspecific genetic variation present within both host and parasite populations (Wakelin, 1978). Since the outcome is determined by the interaction of a finite set of host genes and parasite genes, genetic variation in host susceptibility and parasite infectivity (Richards, 1976; Wakelin, 1978) suggests that more than two outcomes are possible. Variation in host and parasite genomes does not begin and end at the susceptibility/infectivity loci. Other genes may also influence the outcome of host–parasite interactions by altering the life-history patterns of hosts and parasites, and lead to a variety of outcomes.

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Anderson, R. M. (1978). The regulation of host population growth by parasitic species. Parasitology 76, 119–57.
Anderson, R. M. & May, R. M. (1979). Prevalence of schistosome infections within molluscan populations: observed patterns and theoretical predictions. Parasitology 79, 6394.
Anderson, R. M. & May, R. M. (1982). Coevolution of hosts and parasites. Parasitology 85, 411–26.
Baudoin, M. (1975). Host castration as a parasitic strategy. Evolution 29, 335–52.
Becker, W. (1980 a). Metabolic interrelationship of parasitic trematodes and molluscs, especially Schistosoma mansoni in Biomphalaria glabrata. Zeitschrift fur Parasitenkunde 63, 101–11.
Becker, W. (1980 b). Microcalorimetric studies in Biomphalaria glabrata: the influence of Schistosoma mansoni on the basal metabolism. Journal of Comparative Physiology B 135, 101–5.
Bethel, W. M. & Holmes, J. C. (1973). Altered evasive behaviour and responses to light in amphipods harboring acanthocephalan cystacanths. Journal of Parasitology 59, 945–56.
Bethel, W. M. & Holmes, J. C. (1977). Increased vulnerability of amphipods to predation owing to altered behavior induced by larval acanthocephalans. Canadian Journal of Zoology 55, 110–15.
Bousfield, E. L. (1958). Fresh-water amphipod crustaceans of glaciated North America. Canadian Field-Naturalist 72, 55113.
Brassard, P., Rau, M. E. & Curtis, M. A. (1982). Parasite-induced susceptibility to predation in diplostomiasis. Parasitology 85, 495501.
Brown, D. S. (1978). Pulmonate molluscs as intermediate hosts for digenetic trematodes. In Pulmonates, Vol. 2A, Systematics, Evolution and Ecology (ed. Fretter, V. and Peake, J.), pp. 287333. New York: Academic Press.
Carney, W. P. (1969). Behavioral and morphological changes in carpenter ants harboring dicrocoeliid metacercariae. American Midland Naturalist 82, 605–11.
Cheng, T. C. (1971). Enhanced growth as a manifestation of parasitism and shell deposition in parasitized mollusks. In Aspects of the Biology of Symbiosis (ed. Cheng, T. C.), pp. 103–37. Baltimore: University Park Press.
Cheng, T. C., Sullivan, J. T., Howland, K. H., Jones, T. F. & Moran, H. G. (1983). Studies on parasitic castration: soft tissue and shell weights of Ilyanassa obsoleta (Mollusca) parasitized by larval trematodes. Journal of Invertebrate Pathology 42, 143–50.
Chu, K. Y., Sabbaghian, H. & Massoud, J. (1966). Host–parasite relationship of Bulinus truncatus and Schistosoma haematobium in Iran. Bulletin of the World Health Organization 34, 121–30.
Dawkins, R. (1982). The Extended Phenotype. Oxford: Freeman.
Dawkins, R. & Krebs, J. R. (1979). Arms races between and within species. Proceedings of the Royal Society of London., B 205, 489511.
Day, J. F. & Edman, J. D. (1983). Malaria renders mice susceptible to mosquito feeding when gametocytes are most infective. Journal of Parasitology 69, 163–70.
Day, P. R. (1974). Genetics of Host–Parasite Interaction. San Francisco: W. H. Freeman.
Dingle, H. & Hegmann, J. P. (1982). Evolution and Genetics of Life Histories. New York: Springer-Verlag.
Etges, F. J. & Gresso, W. (1965). Effect of Schistosoma mansoni infection upon fecundity in Australorbis glabratus. Journal of Parasitology 51, 757–60.
Ewald, P. W. (1980). Evolutionary biology and the treatment of signs and symptoms of infectious disease. Journal of Theoretical Biology 86, 169–76.
Hairston, N. G. (1973). The dynamics of transmission. In Epidemiology and Control of Schistosomiasis (Bilharziasis) (ed. Ansari, N.), pp. 250336. Baltimore: University Park.
Holmes, J. C. (1983). Evolutionary relationships between parasitic helminths and their hosts. In Coevolution (ed. Futuyma, D. J. and Slatkin, M.), pp. 161–85. Sunderland, Massachusetts: Sinauer.
Holmes, J. C. & Bethel, W. M. (1972). Modification of intermediate host behaviour by parasites. In Behavioral Aspects of Parasite Transmission (ed. Canning, E. U. and Wright, C. A.), pp. 123–49. Zoological Journal of the Linnean Society, Suppl. 1.
James, B. L. (1965). The effects of parasitism by larval Digenea on the digestive gland of the intertidal prosobranch, Littorina saxatilis (Olivi) subsp. tenebrosa (Montagu). Parasitology 55, 93115.
Kuris, A. M. (1980). Effect of exposure to Echinostoma liei miracidia on growth and survival of young Biomphalaria glabrata snails. International Journal for Parasitology 10, 303–8.
Lackie, A. M. (1980). Invertebrate immunity. Parasitology 80, 393412.
Law, R. (1979). Ecological determinants in the evolution of life histories. In Population Dynamics (ed. Anderson, R. M., Turner, B. D. and Taylor, L. R.). London: Blackwell.
Levin, S. A. & Pimentel, D. (1981). Selection of intermediate rates of increase in parasite–host systems. American Naturalist 117, 308–15.
Lie, K. J., Heyniiman, D. & Richards, C. S. (1977). Schistosoma mansoni: temporary reduction of natural resistance in Biomphalaria glabrata induced by irradiated miracidia of Echinostoma paraensei. Experimental Parasitology 43, 5462.
Lo, C. T. (1972). Compatibility and host–parasite relationships between species of the genus Bulinus (Basommatophora: Planorbidae) and an Egyptian strain of Schistosoma haematobium (Trematoda: Digenea). Malacologia 11, 225–80.
Loker, E. S. (1979). Effects of Schistosomatium douthitti infection on the growth, survival, and reproduction of Lymnaea catascopium. Journal of Invertebrate Pathology 34, 138–44.
Mcclelland, G. & Bourns, T. K. R. (1969). Effects of Trichobilharzia ocellata on growth, reproduction, and survival of Lymnaea stagnalis. Experimental Parasitology 24, 137–46.
Mertz, P. B. (1971). Life history phenomena in increasing and decreasing populations. In Symposium on Statistical Ecology, vol. 2 (ed. Patil, G. P., Pielov, E. G. and Waters, W. E.), pp. 351400. University Park, Pennsylvania: Penn State University Press.
Meuleman, E. A. (1972). Host-parasite interrelationships between the freshwater pulmonate Biomphalaria pfeifferi and the trematode Schistosoma mansoni. Netherlands Journal of Zoology 22, 355427.
Minchella, D. J. (1981). Ecological aspects of host-parasite coevolution and their implications in the genetic control of schistosomiasis. Ph.D. thesis, Purdue University, West Lafayette, Indiana, USA.
Minchella, D. J. & Loverde, P. T. (1981). A cost of increased early reproductive effort in the snail Biomphalaria glabrata. American Naturalist 118, 876–81.
Minchella, D. J. & Loverde, P. T. (1983). Laboratory comparison of the relative success of Biomphalaria glabrata stocks which are susceptible and insusceptible to infection with Schistosoma mansoni. Parasitology 86, 335–44.
Mitchell, G. F. (1979). Responses to infection with metazoan and protozoan parasites in mice. Advances in Immunology 28, 451511.
Noble, E. R. & Noble, G. A. (1976). Parasitology: The Biology of Animal Parasites. Philadelphia: Lea & Febiger.
Pan, C. T. (1963). Generalized and focal tissue responses in the snail Australorbis glabratus infected with Schistosoma mansoni. Annals of the New York Academy of Science 113, 475–85.
Pan, C.-T. (1965). Studies on the host-parasite relationship between Schistosoma mansoni and the snail Australorbis glabratus. American Journal of Tropical Medicine and Hygiene 14, 931–76.
Perlowagora-Szumlewicz, A. (1968). The reaction of Australorbis glabratus (Biomphalaria glabrata) to infection with Schistosoma mansoni. Revista do Instituto de Medicina Tropical de Sao Paulo 10, 219–28.
Price, P. W. (1980). Evolutionary Biology of Parasites. Princeton: Princeton University Press.
Richards, C. S. (1975). Genetic factors in susceptibility of Biomphalaria glabrata for different strains of Schistosoma mansoni. Parasitology 70, 231–41.
Richards, C. S. (1976). Genetics of the host–parasite relationship between Biomphalaria glabrata and Schislosoma mansoni. In Genetic Aspects of Host–Parasite Relationships (ed. Taylor, A. E. R. and Muller, H.), pp. 4554. Oxford: Blackwell.
Richards, C. S. & Merritt, J. W. (1972). Genetic factors in susceptibility of juvenile Biomphalaria glabrata to Schistosoma mansoni infection. American Journal of Tropical Medicine and Hygiene 21, 425–34.
Rothschild, M. (1941). Observations on the growth and trematode infections of Peringia ulvae (pennant) 1777 in pool in the Tamar Saltings, Plymouth. Parasitology 33, 406–15.
Schaffer, W. I. & Rosenzweig, M. L. (1978). Homage to the red queen. 1. Coevolution of predators and their victims. Theoretical Population Biology 14, 135–57.
Sluiters, J. F. (1981). Development of Trichobilharzia ocellata in Lymnaea stagnalis and the effects of infection on the reproductive system of the host. Zeitschrift für Parasitenkunde 64, 303–19.
Sluiters, J. F., Brijssaard-Wust, C. M. & Meuleman, E. A. (1980). The relationship between miracidial dose, production of cercariae, and reproductive activity of the host in the combination Trichobilharzia ocellata and Lymnaea stagnalis. Zeitschrift für Parasitenkunde 63, 1326.
Smith Trail, D. R. (1980). Behavioral interactions between parasites and hosts: host suicide and the evolution of complex life cycles. The American Naturalist 116, 7791.
Sturrock, B. M. (1966). The influence of infection with Schistosoma mansoni on the growth rate and reproduction of Biomphalaria pfeifferi. Annals of Tropical Medicine and Parasitology 60, 187–97.
Sturrock, B. M. & Sturrock, R. F. (1970). Laboratory studies of the host–parasite relationship of Schistosoma mansoni and Biomphalaria glabrata from St Lucia, West Indies. Annals of Tropical Medicine and Parasitology 64, 357–63.
Sturrock, R. F. (1973). Field studies on the transmission of Schistosoma mansoni and on the bionomics of its intermediate host, Biomphalaria glabrata, on St Lucia, West Indies. International Journal for Parasitology 3, 175–94.
Tokeson, J. P. E. & Holmes, J. C. (1982). The effects of temperature and oxygen on the development of Polymorphusmarilis (Acanthocephala) in Gammarus lacustris (Amphipoda). Journal of Parasitology 68, 112–19.
Ulmer, M. J. (1971). Site-finding behavior in helminths in intermediate and definitive hosts. In Ecology and Physiology of Parasites (ed. Fallis, A. M.), pp. 123–59. Toronto: University of Toronto Press.
Vinson, S. B. & Iwantsch, G. F. (1980). Host regulation by insect parasitoids. The Quarterly Review of Biology 55, 143–65.
Waage, J. K. (1979). The evolution of insect/vertebrate associations. Biological Journal of the Linnean Society 12, 187224.
Wakelin, D. (1978). Genetic control of susceptibility and resistance to parasitic infection. Advances in Parasitology 16, 219308.
Webbe, G. & James, C. (1972). Host-parasite relationships of Bulinus globosus and B. truncatus with strains of Schistosoma haematobium. Journal of Helminthology 46, 185–99.
Wickler, W. (1968). Mimicry in Plants and Animals. New York: McGraw-Hill.
Wickler, W. (1976). Evolution-oriented ethology, kin selection, and altruistic parasites. Zeitschrift für Tierpsychologie 42, 206–14.
Williams, C. L. & Gilbertson, D. E. (1983). Altered feeding response as a cause for the altered heartbeat rate and locomotor activity of Schistosoma mansoni-infected Biomphalaria glabrata. Journal of Parasitology 69, 671–6.
Wilson, F. A. & Denison, J. (1980). The parasitic castration and gigantism of Lymnaea truncatula infected with the larval stages of Fasciola hepatica. Zeitschrift für Parasitenkunde 61, 109–19.
Wright, C. A. (1966). The pathogenesis of helminths in the mollusca. Helminthological Abstrasts 35, 207–24.
Wright, C. A. (1971 a). Flukes and Snails. London: Allen and Unwin Ltd.
Wright, C. A. (1971 b). Review of Genetics of a Molluscan Vector of Schistosomiasis by C. S. Richards. Tropical Disease Bulletin 68, 333–5.
Yamaguti, S. (1958). Systema Helminthum: Vol. I, The Digenetic Trematodes of Vertebrates. New York: Interscience Publishers, Inc.
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