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Genetic variability in parasites and host—parasite interactions

Published online by Cambridge University Press:  06 April 2009

R. C. A. Thompson  and
A. J. Lymbery
R. C. A. Thompson
Affiliation:
Institute for Molecular Genetics and Animal Disease and WHO Collaborating Centre for the Molecular Epidemiology of Parasitic Infections, School of Veterinary Studies, Murdoch University, Murdoch, Western Australia, Australia6150
A. J. Lymbery
Affiliation:
Western Australian Department of Agriculture, Bunbury, Western Australia, Australia, 6230
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Summary

We have examined genetic variability in parasites in the context of ecological interactions with the host. Recent research on Echinococcus, Giardia and Cryptosporidium has been used to illustrate: (i) the problems that parasite variability and species recognition pose for understanding the complex and often controversial relationship between parasite and host occurrence; (ii) the need for accurate parasite characterization and the application of appropriate molecular techniques to studies on parasite transmission if fundamental questions about zoonotic relationships and risk factors are to be answered; (iii) our lack of understanding about within-host interactions between genetically heterogeneous parasites at the inter-and intraspecific levels, and the significance of such interactions with respect to evolutionary considerations and the clinical outcome of parasite infections. If advances in molecular biology and mathematical ecology are to be realized, we need to give serious consideration to the development of appropriate species concepts and in vivo systems for testing the predictions and assumptions of theoretical models.

Keywords

EchinococcusGiardiaCryptosporidiumgenetic variationmolecular characterizationhost occurrencespecies recognitionepidemiologyecological interactionsevolutionvirulence
Type
Research Article
Information
Parasitology , Volume 112 , Supplement S1: Symposia of the British Society for Parasitology Volume 33:Genetics of host and parasite: implications for immunity, epidemiology and evolution , March 1996 , pp. S7 - S22
Copyright
Copyright © Cambridge University Press 1996

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References

Alpert, G. L. B., Bell, C. E., Kirkpatrick, L. D., Budnick, J. M., Campos, H. M., Friedman, H. M. & Plotkin, S. A. (1986). Outbreak of cryptosporidiosis in a day-care centre. Pediatrics 77, 152–6.Google Scholar
Anderson, R. M. & May, R. M. (1992). Infectious Disease of Humans: Dynamics and Control. Oxford: Oxford University Press.Google Scholar
Anderson, T. J. C., Romero-Abal, M. E. & Jaenike, J. (1995). Mitochondrial DNA and Ascaris microepidemiology: the composition of parasite populations from individual hosts, families and villages. Parasitology 110, 221–9.Google Scholar
Andrews, R. H., Adams, M., Boreham, P. F. L., Mayrhofer, G. & Meloni, B. P. (1989). Giardia intestinalis: Electrophoretic evidence for a species complex. International Journal for Parasitology 19, 183–90.Google Scholar
Binz, N., Thompson, R. C. A., Lymbery, A. J. & Hobbs, R. P. (1992). Comparative studies on the growth dynamics of genetically distinct isolates of Giardia duodenalis in vitro. International Journal for Parasitology 22, 195–202.Google Scholar
Bonhoeffer, s. & Nowak, M. A. (1994). Mutation and the evolution of virulence. Proceedings of the Royal Society of London B 258, 133–40.Google Scholar
Boreham, P. F. L., Phillips, R. E. & Shepherd, R. W. (1987). Heterogeneity in the responses of clones of Giardia intestinalis to anti-giardial drugs. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 406–7.Google Scholar
Bowles, J., Blair, D. & McManus, D. P. (1995). A molecular phylogeny of the genus Echinococcus. Parasitology 110, 317–28.CrossRefGoogle ScholarPubMed
Bremermann, H. J. & Pickering, J. (1983). A gametheoretical model of parasite virulence. Journal of Theoretical Biology 100, 411–26.Google Scholar
Bull, J. J. (1994). Evolution of Virulence. Evolution 48, 1423–37.Google Scholar
Bulmer, M. G. (1971). Stable equilibria under the two-island model. Heredity 27, 321–30.Google Scholar
Casemore, D. P. (1990). Epidemiological aspects of human cryptosporidiosis. Epidemiology and Infection 104, 1–28.CrossRefGoogle ScholarPubMed
Constantine, C. C., Lymbery, A. J., Thompson, R. C. A. & Obendorf, D. L. (1991). The origin of a new focus of infection with Echinococcus granulosus in Tasmania. International Journal for Parasitology 21, 959–61.Google Scholar
Constantine, C. C., Thompson, R. C. A., Jenkins, D. J., Hobbs, R. P. & Lymbery, A. J. (1993). Morphological characterization of adult Echinococcus granulosus as a means of determining transmission patterns. Journal of Parasitology 79, 57–61.Google Scholar
Cracraft, J. (1983). Species concepts and speciation analysis. In Current Ornithology, (ed. Johnston, R. F.) Vol. 1. pp. 159–87. New York: Plenum Press.Google Scholar
Crawford, F. G., Vermund, S. H., Ma, J. Y. & Deckelbaum, R. J. (1988). Asymptomatic cryptosporidiosis in a New York City day care centre. Paediatric Infectious Diseases Journal 7, 806.CrossRefGoogle Scholar
Current, W. L. & Reese, N. C. (1986). A comparison of endogenous development of three isolates of Cryptosporidium in suckling mice. Journal of Protozoology 33, 98–108.CrossRefGoogle ScholarPubMed
Dame, J. B., Blouin, M. S. & Courtney, C. H. (1993). Genetic structure of populations of Ostertagia ostertagi. Veterinary Parasitology 46, 55–62.Google Scholar
Day, K. P., Koella, J. C., Nee, S., Gupta, S. & Read, A. F. (1992). Population genetics and dynamics of Plasmodium falciparum: an ecological view. Parasitology 104, S35–S52.Google Scholar
Deplazes, P., Thompson, R. C. A. & Penhale, W. J. (1994). Primary infection of dogs with Echinococcus granulosus: systemic and local (Peyer's patches) immune responses. Veterinary Immunology and Immunopathology 40, 171–84.CrossRefGoogle ScholarPubMed
De Queiroz, K. & Donoghue, M. J. (1988). Phylogenetic systematics and the species problem. Cladistics 4, 317–18.CrossRefGoogle ScholarPubMed
De Queiroz, K. & Donoghue, M. J. (1990). Phylogenetic systematics or Nelson's version of cladistics?. Cladistics 6, 61–75.Google Scholar
Diers, J. & McCallister, G. L. (1989). Occurrence of Cryptosporidium in home daycare centres in west-central Colorado. Journal of Parasitology 75, 637–8.CrossRefGoogle ScholarPubMed
Dubey, J. P., Speer, C. A. & Fayer, R. (1990). General Biology of Cryptosporidium. In Cryptosporidiosis of Man and Animals, (ed. Dubey, J. P., Speer, C. A. & Payer, R.), pp. 1–29. Boca Raton: CRC Press.Google Scholar
Ebert, D. (1994). Genetic differences in the interactions of a microsporidian parasite and four clones of its cyclically parthenogenetic host. Parasitology 108, 11–16.Google Scholar
Eckert, J., Thompson, R. C. A., Michael, S. A., Kumaratilake, L. M. & El-Sawah, H. M. (1989). Echinococcus granulosus of camel origin: Development in dogs and parasite morphology. Parasitology Research 75, 536–44.Google Scholar
Ehrlich, P. R. & Raven, p. H. (1969). Differentiation of populations. Science 165, 1228–32.Google Scholar
Ewald, P. W. (1988). Cultural vectors, virulence, and the emergence of evolutionary epidemiology. Oxford Surveys in Evolutionary Biology 5, 215–45.Google Scholar
Farbey, M. D., Reynoldson, J. A. & Thompson, R. C. A. (1995). In vitro drug susceptibility of 29 isolates of Giardia duodenalis from humans. International Journal for Parasitology 25, 593–9.Google Scholar
Fayer, R. & Ungar, B. L. P. (1986). Cryptosporidium spp and Cryptosporidiosis. Microbiology Review 50, 458–83.Google Scholar
Filice, F. p. (1952). Studies on the cytology and life history of Giardia from the laboratory rat. University of California Publications in Zoology 57, 53–146.Google Scholar
Frank, S. A. (1994). Recognition and polymorphism in host–parasite genetics. Philosophical Transactions of the Royal Society of London B 346, 283–93.Google Scholar
Gupta, S., Trenholme, K., Anderson, R. M. & Day, K. P. (1994). Antigenic diversity and the transmission dynamics of Plasmodium falciparum. Science 263, 961–3.Google Scholar
Hall, M. L., Costa, N. D., Thompson, R. C. A., Lymbery, A. J., Meloni, B. P. & Wales, R. G. (1992). Genetic variants of Giardia duodenalis differ in their metabolism. Parasitology Research 78, 712–14.Google Scholar
Hanna, J., & Brookes, D. (1995). Cryptosporidiosis in a child day-care centre. Communicable Disease Intelligence 19, 6–8.Google Scholar
Harvey, P. H. & Nee, S. (1994). Phylogenetic epidemiology lives. Trends in Ecology and Evolution 9, 361–3.Google Scholar
Hassell, M. P., Comins, H. N. & May, R. M. (1994). Species coexistence and self-organising spatial dynamics. Nature 370, 290–2.Google Scholar
Hide, G. & Tait, A. (1991). The molecular epidemiology of parasites. Experientia 47, 128–43.Google Scholar
Hobbs, R. P., Lymbery, A. J. & Thompson, R. C. A. (1990). Rostellar hook morphology of Echinococcus granulosus (Batsch, 1786) from natural and experimental Australian hosts, and its implications for strain recognition. Parasitology 101, 273–81.Google Scholar
Holmes, E. C. & Garnett, G. P. (1994). Genes, trees and infections: molecular evidence in epidemiology. Tree 9, 256–60.Google ScholarPubMed
Holmes, J. C. (1990). Competition, contacts, and other factors restricting niches of parasitic helminths. Annales de Parasitologie Humaine et Comparee 65, 69–72.Google Scholar
Hope, M., Bowles, J. & McManus, D. P. (1991). A reconsideration of the Echinococcus granulosus strain situation in Australia following RFLP analysis of cystic material. International Journal for Parasitology 21, 471–5.Google Scholar
Hudson, R. R. (1990). Gene genealogies and the coalescent process. Oxford Surveys in Evolutionary Biology 7, 1–44.Google Scholar
Kamiya, M. & Sato, H. (1990 a). Survival, strobilation and sexual maturation of Echinococcus multilocularis in the small intestine of golden hamsters. Parasitology, 100, 125–30.Google Scholar
Kamiya, M. & Sato, H. (1990 b). Complete life cycle of the canid tapeworm, Echinococcus multilocularis, in laboratory rodents. FASEB Journal 4, 3334–9.CrossRefGoogle ScholarPubMed
Kammerer, W. S. & Schantz, P. M. (1984). Long term follow-up of human hydatid disease (Echinococcus granulosus) treated with a high-dose mebendazole regimen. American Journal of Tropical Medicine and Hygiene 33, 132–7.Google Scholar
Kumaratilake, L. M. & Thompson, R. C. A. (1982). A review of the taxonomy and speciation of the genus Echinococcus. Zeitschrift für Parasitenkunde 68, 121–46.Google Scholar
Kumaratilake, L. M., Thompson, R. C. A. & Dunsmore, J. D. (1983). Comparative strobilar development of Echinococcus granulosus of sheep origin from different geographical areas of Australia in vivo and in vitro. International Journal for Parasitology 13, 151–6.CrossRefGoogle ScholarPubMed
Kumaratilake, L. M. & Thompson, R. C. A. (1984). Morphological characterisation of Australian strains of Echinococcus granulosus. International Journal for Parasitology 14, 467–77.Google Scholar
Levine, N. D. (1984). Taxonomy and review of the coccidian genus Cryptosporidium (Protozoa, Apicomplexa). Journal of Protozoology 31, 94–8.Google Scholar
Lymbery, A. J. (1992). Interbreeding, monophyly and the genetic yardstick: species concepts in parasites. Parasitology Today 8, 208–11.Google Scholar
Lymbery, A. J. (1995). Genetic diversity, genetic differentiation and speciation in the genus Echinococcus Rudolphi 1801. In Echinococcus and Hydatid Disease, (eds. Thompson, R. C. A. & Lymbery, A. J.), pp. 51–87. Wallingford: CAB International.Google Scholar
Lymbery, A. J. & Thompson, R. C. A. (1988). Electrophoretic analysis of genetic variation in Echinococcus granulosus from domestic hosts in Australia. International Journal for Parasitology 18, 803–11.Google Scholar
Lymbery, A. J. & Thompson, R. C. A. (1989). Genetic differences between cysts of Echinococcus granulosus from the same host. International Journal for Parasitology 19, 961–4.CrossRefGoogle ScholarPubMed
Lymbery, A. J., Thompson, R. C. A. & Hobbs, R. P. (1990). Genetic diversity and genetic differentiation in Echinococcus granulosus (Batsch, 1786) from domestic and sylvatic hosts on the mainland of Australia. Parasitology 101, 283–9.Google Scholar
Majewska, A. C., Kasprzak, W., Dejonckheere, J. F. & Kaczmarek, E. (1991). Heterogeneity in the sensitivity of stocks and clones of Giardia to metronidazole and ornidazole. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 67–9.Google Scholar
May, R. M. & Nowak, M. A. (1994). Superinfection, metapopulation dynamics and the evolution of diversity. Journal of Theoretical Biology 170, 95–114.Google Scholar
Mayr, E. (1942). Systematics and the origin of Species. New York: Columbia University Press.Google Scholar
Mayr, E. (1974). The challenge of diversity. Taxon 23, 3–9.Google Scholar
McDonald, v., Deer, R. M. A., Nina, J. M. S., Wright, S., Chiodini, P. L. & McAdam, K. P. W. J. (1991). Characterisation and specificity of hybridoma antibodies against oocyst antigens of Cryptosporidium parvum from man. Parasite Immunology 13, 251–9.Google Scholar
McInnes, L. M. (1994). Phenotypic Characterisation of the Differential Sensitivity of Giardia Isolates to Drugs. Honors Thesis, Murdoch University, Western Australia.Google Scholar
McManus, D. P. & Bryant, C. (1995). Biochemistry, physiology and molecular biology of Echinococcus. In Echinococcus and Hydatid Disease, (eds. Thompson, R. C. A. & Lymbery, A. J.), pp. 135–81. Wallingford: CAB International.Google ScholarPubMed
McManus, D. P. & Smyth, J. D. (1982). Intermediary carbohydrate metabolism in protoscoleces of Echinococcus granulosus (horse and sheep strains) and E. multilocularis. Parasitology 84, 351–66.CrossRefGoogle ScholarPubMed
Mead, J. R., Humphreys, R. C., Sammons, D. W. & Sterling, C. R. (1990). Identification of isolate specific sporozoite proteins of Cryptosporidium parvum by two-dimensional gel electrophoresis. Infection and Immunity 58, 2071–5.Google Scholar
Meloni, B. P., Lymbery, A. J. & Thompson, R. C. A. (1988). Isoenzyme analysis of 30 isolates of Giardia from humans and lower animals. American Journal of Tropical Medicine and Hygiene 38, 65–73.Google Scholar
Meloni, B. P., Lymbery, A. J. & Thompson, R. C. A. (1995). Genetic characterization of isolates of Giardia duodenalis by enzyme electrophoresis: implications for reproductive biology, population structure, taxonomy and epidemiology. Journal of Parasitology 81, 368–83.Google Scholar
Meloni, B. P., Thompson, R. C. A., Eckert, J., Kohler, P. & Stranden, A. M. (1992). Critical comparison of Giardia duodenalis from Australia and Switzerland using isoenzyme electrophoresis. Acta Tropica 50, 115–24.Google Scholar
Morgan, U. M., Constantine, C. C., Greene, W. K. & Thompson, R. C. A. (1993). RAPD (random amplified polymorphic DNA) analysis of Giardia DNA and correlation with isoenzyme data. Transactions of the Royal Society of Tropical Medicine and Hygiene 87, 702–5.Google Scholar
Morgan, U. M., Constantine, C. C., O'Donoghue, P., O'Brien, p. A. & Thompson, R. C. A. (1995). RAPD (random amplified polymorphic DNA) analysis of Cryptosporidium isolates. American Journal of Tropical Medicine and Hygiene 52, 559–64.CrossRefGoogle ScholarPubMed
Nash, T. E., McCutchan, T., Keister, D., Dame, J. B., Conrad, J. D. & Gillin, F. D. (1985). Restriction-endonuclease analysis of DXA from 15 Giardia isolates obtained from humans and animals. Journal of Infectious Diseases 152, 64–73.Google Scholar
Nichols, G. L., McLauchlin, J. & Samuel, D. (1991). A technique for typing Cryptosporidium isolates. Journal of Protozoology 38, 237S–40S.Google Scholar
Nina, J. M. S., McDonald, V., Deer, R. M. A., Wright, S. E., Dyson, D. A., Chiodini, P. L. C. & McAdam, K. P. W. J. (1992). Comparative study of the antigenic composition of oocyst isolates of Cryptosporidium parvum from different hosts. Parasite Immunology 14, 227–32.Google Scholar
Nixon, K. C. & Wheeler, Q. D. (1990). An amplification of the phylogenetic species concept. Cladistics 6, 211–23.Google Scholar
Nowak, M. A. & May, R. M. (1994). Superinfection and the evolution of parasite virulence. Proceedings of the Royal Society of London B 255, 81–9.Google Scholar
O'donoghue, P. J. (1995). Cryptosporidium and Cryptosporidiosis in man and animals. International Journal for Parasitology 25, 139–95.Google Scholar
Ortega, Y. R., Sheehy, R. R., Cama, V. A., Oishi, K. K. & Sterling, C. R. (1991). Restriction fragment length polymorphism analysis of Cryptosporidium parvum isolates of bovine and human origin. Journal of Protozoology 38, 40S–1S.Google Scholar
Paterson, H. E. H. (1985). The recognition concept of species. In Species and speciation (ed. Vrba, E. S.), pp. 21–9. Pretoria: Transvaal Museum.Google Scholar
Pozio, E., Morales, M. A. G., Barbieri, F. M. & la Rosa, G. (1992). Cryptosporidium: different behaviour in calves of isolates of human origin. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 636–8.CrossRefGoogle ScholarPubMed
Price, P. W. (1980). Evolutionary Biology of Parasites. Princeton: Princeton University Press.Google Scholar
Proctor, E. M., Isaac-Renton, J. L., Boyd, J., Wong, Q. & Bowie, W. R. (1989). Isoenzyme analysis of human and animal isolates of Giardia duodenalis from British Columbia, Canada. American Journal of Tropical Medicine and Hygiene 41, 411–15.Google Scholar
Rosen, D. E. (1979). Fishes from the uplands and intermontane basins of Guatemala: revisionary studies and comparative geography. Bulletin of the American Museum of Natural History 162, 267–376.Google Scholar
Rossi, V., Wincker, P., Ravel, C., Blaineau, C., Pagés, M. & Bastien, P. (1994). Structural organisation of microsatellite families in the Leishmania genome and polymorphisms at two (CA)n loci. Molecular and Biochemical Parasitology 65, 271–82.Google Scholar
Saimot, A. G., Meulemans, A., Hay, J. M., Mohler, J., Manuel, C. & Coulaud, J. P. (1981). Etude pharmacocinetique du flubendazole au cours de l'hydatidose humaine a E. granulosus. Résultats préliminaires. Nouvelle Presse Medicate 10, 3121–4.Google Scholar
Schantz, P. M., Van den Bossche, H. & Eckert, J. (1982). Chemotherapy for larval echinococcosis in animals and humans: report of a workshop. Zeithschrift für Parasitenkunde 67, 5–26.CrossRefGoogle ScholarPubMed
Sebens, K. P. & Thorne, B. L. (1985). Coexistence of clones, clonal diversity, and the effects of disturbance. In Population Biology and Evolution of Clonal Organisms (ed. Jackson, J. B. C., Buss, L. W. & Cook, R. E.), pp. 357–98. New Haven: Yale University Press.Google Scholar
Severson, D. W. (1994). Applications of molecular marker analysis to mosquito vector competence. Parasitology Today 10, 336–40.Google Scholar
Shabovskaya, E. A., Bulgakov, V. A., Ponomareva, V. E., Dariko, O. P., Voloshchuk, S. D. & Kikot, V. II, (1989). Hydatidosis in the Ukranian SSR. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 6, 49–51 (In Russian).Google Scholar
Simmons, N. A. (1991). Cryptosporidium and Giardia lamblia. Biologist 38, 147–8.Google Scholar
Smyth, J. D. (1987). Changing concepts in the microecology, macroecology and epidemiology of hydatid disease. In Helminth Zoonoses (ed. Geerts, S., Kumar, V. & Brandt, J), pp. 1–11. Dordrecht: Martinus Nijhoff.Google Scholar
Sokal, R. R. & Crovello, T. J. (1970). The biological species concept: a critical evaluation. American Naturalist 104, 127–53.Google Scholar
Sousa, W. P. (1994). Patterns and processes in communities of helminth parasites. Trends in Ecology and Evolution 9, 52–7.Google Scholar
Tavare, S. (1984). Line-of-descent and genealogical processes, and their applications in population genetics models. Theoretical Population Biology 26, 119–64.Google Scholar
Templeton, A. R. (1989). The meaning of species and speciation: a genetic perspective. In Speciation and its Consequences (ed. Otte, D. & Endler, J. A.), pp. 3–27. Sunderland, Massachusetts: Sinauer Associates.Google Scholar
Thompson, R. C. A. (1991). Echinococcus and Giardia: variation on a theme. International Journal for Parasitology 21, 291–7.Google Scholar
Thompson, R. C. A. (1992). Parasitic zoonoses: problems created by people, not animals. International Journal for Parasitology 22, 555–62.Google Scholar
Thompson, S. C. (1994). Infectious diarrhoea in children. Controlling transmission in the child care setting. Journal of Paediatric Child Health 30, 210–19.CrossRefGoogle ScholarPubMed
Thompson, R. C. A. (1995). Biology and systematics of Echinococcus. In Echinococcus and Hydatid Disease (ed. Thompson, R. C. A. and Lymbery, A. J.), pp. 1–50. Wallingford: CAB InternationalGoogle Scholar
Thompson, R. C. A. & Eckert, J. (1983). Observations on Echinococcus multilocularis in the definitive host. Zeitschrift für Parasitenkunde 69, 335–45.Google Scholar
Thompson, R. C. A., Kumaratilake, L. M. & Eckert, J. (1984). Observations on Echinococcus granulosus of cattle origin in Switzerland. International Journal for Parasitology 14, 283–91.Google Scholar
Thompson, R. C. A. & Lymbery, A. J. (1988). The nature, extent and significance of variation within the genus Echinococcus. Advances in Parasitology 27, 210–58.Google ScholarPubMed
Thompson, R. C. A. & Lymbery, A. J. (1990). Intraspecific variation in parasites – what is a strain?. Parasitology Today 6, 345–8.Google Scholar
Thompson, R. C. A. & Lymbery, A. J. (1991). The epidemiological significance of biological variation in Echinococcus. Archives de la Hidatidosis 30, 195–200.Google Scholar
Thompson, R. C. A. & Lymbery, A. J. (1994). Genetic variation in helminths and its epidemiological significance. In Helminthology (ed. Chowdhury, N. & Tada, I.), pp. 146–59. New Delhi: Narosa Publishing House.Google Scholar
Thomson, R. C. A., Lymbery, A. J. & Meloni, B. P. (1990). Genetic variation in Giardia Kunstler, 1882: taxonomic and epidemiological significance. Review article. Protozoological Abstracts 14, 1–28.Google Scholar
Thompson, R. C. A., Lymbery, A. J., Meloni, B. P., Morgan, V. M., Binz, N., Constantine, C. C. & Hopkins, R. M. (1994). Molecular epidemiology of parasite infections. In Biology of Parasitism, (ed. Ehrlich, R. & Nieto, A.), pp. 167–85. Montevideo, Uruguay: Edicio Trilce.Google Scholar
Thompson, R. C. A., Lymbery, A. J. & Constantine, C. C. (1995). Variation in Echinococcus: towards a taxonomic revision of the genus. Advances in Parasitology 35, 145–76.Google Scholar
Thompson, R. C. A. & Meloni, B. p. (1993). Molecular variation in Giardia and its implications. Acta Tropica 53, 167–84.Google Scholar
Thompson, R. C. A., Reynoldson, J. A. & Mendis, A. H. W. (1993). Giardia and giardiasis. Advances in Parasitology 32, 71–160.Google Scholar
Thompson, R. C. A. & Smyth, J. D. (1975). Equine hydatidosis: a review of the current status in Great Britain and the results of an epidemiological survey. Veterinary Parasitology 1, 107–27.Google Scholar
Tibayrenc, M. & Ayala, F. J. (1988). Isozyme variability in Trypanosoma cruzi, the agent of Chagas' disease: genetical, taxonomical, and epidemiological significance. Evolution 42, 277–92.Google Scholar
Tibayrenc, M., Kjelberg, F. & Ayala, F. J. (1991). The clonal theory of parasitic protozoa. Bioscience 41, 767–74.Google Scholar
Upcroft, P., Mitchell, R. & Boreham, P. F. L. (1990). DNA fingerprinting of the intestinal parasite Giardia duodenalis with the M13 phage genome. International Journal for Parasitology 20, 319–23.Google Scholar
Wachira, T. M., Bowles, J., Zeyhle, E. & McManus, D. P. (1993). Molecular examination of the sympatry and distribution of sheep and camel strains of Echinococcus granulosus in Kenya. American Journal of Tropical Medicine and Hygiene 48, 473–9.Google Scholar
Weider, L. J. (1992). Disturbance, competition and the maintenance of clonal diversity in Daphnia pulex. Journal of Evolutionary Biology 5, 505–22.Google Scholar
Weiss, J. B., Van Keulen, H. & Nash, T. E. (1992). Classification of subgroups of Giardia lamblia based upon ribosomal RNA gene sequence using the polymerase chain reaction. Molecular and Biochemical Parasitology 54, 73–86.CrossRefGoogle ScholarPubMed
Wiley, E. O. (1978). The evolutionary species concept reconsidered. Systematic Zoology 27, 17–26.Google Scholar
Wilson, C. C. & Herbert, P. D. N. (1992). The maintenance of taxon diversity in an asexual assemblage: an experimental analysis. Ecology 73, 1462–72.Google Scholar
Wright, S. (1951). The genetical structure of population. Annals of Eugenics 15, 323–54.Google Scholar