Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-24T12:25:59.392Z Has data issue: false hasContentIssue false
  • English
  • Français

Virulence of lizard malaria: the evolutionary ecology of an ancient parasite—host association

Published online by Cambridge University Press:  06 April 2009

J. J. Schall
J. J. Schall
Affiliation:
Department of Zoology, University of Vermont, Burlington, Vermont 05405, USA
Get access Rights & Permissions [Opens in a new window]

Summary

The negative consequences of parasitic infection (virulence) were examined for two lizard malaria parasite—host associa tions: Plasmodium agamae and P. giganteum, parasites of the rainbow lizard, Agama agania, in Sierra Leone, West Africa; and P. mexicanum in the western fence lizard, Sceloporus occidentalis, in northern California. These malaria species vary greatly in their reproductive characteristics: P. agamae produces only 8 merozoites per schizont, P. giganteum yields over 100, and P. mexicanum an intermediate number. All three parasites appear to have had an ancient association with their host. In fence lizards, infection with malaria is associated with increased numbers of immature erythrocytes, decreased haemoglobin levels, decreased maximal oxygen consumption, and decreased running stamina. Not affected were numbers of erythrocytes, resting metabolic rate, and sprint running speed which is supported by anaerobic means in lizards. Infected male fence lizards had smaller testes, stored less fat in preparation for winter dormancy, were more often socially submissive and, unexpectedly, were more extravagantly coloured on the ventral surface (a sexually dimorphic trait) than non-infected males. Females also stored less fat and produced smaller clutches of eggs, a directly observed reduction in fitness. Infected fence lizards do not develop behavioural fevers. P. mexicanum appears to have broad thermal buffering abilities and thermal tolerance; the parasite's population growth was unaffected by experimental alterations in the lizard's body temperature. The data are less complete for A. agama, but infected lizards suffered similar haematological and physiological effects. Infected animals may be socially submissive because they appear to gather less insect prey, possibly a result of being forced into inferior territories. Infection does not reduce clutch size in rainbow lizards, but may lengthen the time between clutches. These results are compared with predictions emerging from several models of the evolution of parasite virulence. The lack of behavioural fevers in fence lizards may represent a physiological constraint by the lizards in evolving a thermal tolerance large enough to allow elimination of the parasite via fever. Such constraints may be important in determining the outcome of parasite—host coevolution. Some theory predicts low virulence in old parasite—host systems and higher virulence in parasites with greater reproductive output. However, in conflict with this argument, all three malarial species exhibited similar high costs to their hosts.

Keywords

lizard malariaparasite virulencePlasmodiumlizard ecology
Type
Research Article
Information
Parasitology , Volume 100 , Issue S1: Symposia of the British Society for Parasitology Volume 27:The evolutionary biology of parasitism , June 1990 , pp. S35 - S52
Copyright
Copyright © Cambridge University Press 1990

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

Alger, N. E., Branton, M., Harant, J. & Silverman, P. H. (1971). Plasmodium berghei NK65 in the inbred A/J mouse: variations in virulence of P. berghei demes. Journal of Protozoology 18, 598–601.Google Scholar
Aragao, H. D. B. & Neiva, A. (1909). A contribution to the study of the intraglobular parasites of the lizards. Two new species of Plasmodium, P1. diploglossi n.sp. and P1. tropiduri n.sp. Memórias do Instituto Oswaldo Cruz 1, 44–50.CrossRefGoogle Scholar
Ayala, S. C. (1970). Lizard malaria in California; description of a strain of Plasmodium mexicanum, and biogeography of lizard malaria in western North America. Journal of Parasitology 56, 417–25.Google Scholar
Ayala, S. C. (1978). Checklist, host index, and annotated bibliography of Plasmodium from reptiles. Journal of Protozoology 25, 87–100.CrossRefGoogle ScholarPubMed
Bennett, A. F. (1983). Ecological consequences of activity metabolism. In Lizard Ecology (ed. Huey, R. B., Pianka, E. R. & Schoener, T. W.), pp. 11–23. Cambridge, MA: Harvard University Press.CrossRefGoogle Scholar
Bonorris, J. S. & Ball, G. H. (1955). Schellackia occidentalis n.sp., a blood-inhabiting coccidian found in lizards in southern California. Journal of Protozoology 2, 31–4.CrossRefGoogle Scholar
Boorstein, S. M. & Ewald, P. W. (1987). Costs and benefits of behavioral fever in Melanoplus sanguinipes infected by Nosemea acridophagus. Physiological Zoology 60, 586–95.Google Scholar
Bromwich, C. R. & Schall, J. J. (1986). Infection dynamics of Plasmodiurn mnexicanum, a malarial parasite of lizards. Ecology 67, 1227–35.Google Scholar
Bruce-Chwatt, L. J. (1985). Essential Malariology. New York: John Wiley & Sons.Google Scholar
Burnet, M. & White, D. O. (1972). Natural History of Infectious Disease. Cambridge: Cambridge University Press.Google Scholar
Caldwell, F. E. (1944). In vitro effects of high temperature on avian malarial parasites. Journal of Infectious Diseases 74, 189–205.CrossRefGoogle Scholar
Chaniotis, B. N. & Anderson, J. R. (1968). Age structure, population dynamics and vector potential of Phlebotomus in northern California. Journal of Medical Entomology 5, 273–92.CrossRefGoogle ScholarPubMed
Coatney, C. R., Collins, W. E., Warren, M. & Contacos, P. G. (1971). The Primate Malarias. Bethesda, Maryland: United States Department of Health, Education, and Welfare.Google Scholar
Dunn, M. J. (1969). Alterations of red blood cell metabolism in simian malaria: evidence for abnormalities of nonparasitized cells. Military Medicine 134, 1100–5.CrossRefGoogle ScholarPubMed
Ewald, P. W. (1983). Host—parasite relations, vectors, and the evolution of disease severity. Annual Review of Ecology and Systematics 14, 465–85.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
Garnham, P. C. C. (1980). Malaria in its various vertebrate hosts. In Malaria, Vol. 1 (ed. Kreier, J. P.), pp. 95–144. New York: Academic Press.Google Scholar
Gill, D. E. & Mock, B. A. (1985). Ecological and evolutionary dynamics of parasites: the case of Trypanososna diemyctyli in the red-spotted newt Notophthalmus viridescens. In Ecology and Genetics of Host—Parasite Interactions (ed. Rollinson, D. & Anderson, R. M.), pp. 157–83. London: Academic Press.Google Scholar
Gould, S. J. (1989). A developmental constraint in Cerion, with comments on the definition and interpretation of constraint in evolution. Evolution 43, 516–39.Google ScholarPubMed
Hahn, W. K. & Tinkle, D. W. (1965). Fat body cycling and experimental evidence for its adaptive significance to ovarian follicle development in the lizard Uta stansburiana. Journal of Experimental Zoology 158, 79–86.Google Scholar
Hamilton, W. D. & Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384–7.Google Scholar
Hoeprich, P. D. (1977). Host—parasite relationships and the pathogenesis of infectious disease. In Infectious Diseases (ed. Hoeprich, P. D.), pp. 34–45. New York: Harper & Row.Google Scholar
Keymer, A. & Read, A. (1989). Behavioral ecology: the impact of parasitism. In Parasitism: Coexistence or Conflict? (ed. Toft, C. A. & Aeschlimann, A.). London: Oxford University Press (in the Press).Google Scholar
Klein, T. A., Akin, D. C., Young, D. O., Telford, S. R. & Butler, A. F. (1988). Sporogony, development and ultrastructure of extrinsic stages of Plasmodiunz mexicanum. International Journal for Parasitology 18, 463–76.Google Scholar
Kluger, J. J. (1979). Fever. Princeton: Princeton University Press.Google Scholar
Landau, I. & Boulard, Y. (1978). Life cycles and morphology. In Rodent Malaria (ed. Kendrick, Killick R. & Peters, W.), pp. 53–84. London: Academic Press.Google Scholar
Lewontin, R. C. (1970). The units of selection. Annual Review of Ecology and Systematics 1, 1–18.CrossRefGoogle Scholar
Maegralth, B. & Fletcher, A. (1972). The pathogenesis of mammalian malaria. In Advances in Parasitology, Vol. 10 (ed. Dawes, B.), pp. 49–75. New York: Academic Press.Google Scholar
Maizels, C. S. (1980). The cell kinetics of the peripheral blood of the Aruban whiptail lizard, Cnemidophorus arubensis. Thesis, Immaculate Heart College.Google Scholar
Manwell, R. D. (1955). Some evolutionary possibilities in the history of the malaria parasites. Indian Journal of Malariology 9, 247–53.Google ScholarPubMed
Manwell, R. D. (1977). Gregarines and haemogregarines. In Parasitic Protozoa, Vol. 3 (ed. Kreier, J. P.), pp. 1–32. New York: Academic Press.Google Scholar
Moreau, R. E. (1963). Vicissitudes of the African biomes in the late Pleistocene. Proceedings of the Zoological Society of London 141, 395–421.CrossRefGoogle Scholar
Nussenzweig, R. S., Cochrane, A. H. & Lustig, H. J. (1978). Immunological responses. In Rodent Malaria (ed. Killick-Kendrick, R. & Peters, W.), pp. 247–307. London: Academic Press.Google Scholar
Petit, C., Landau, I., Boulard, Y., Gomes, A. & Touratier, L. (1983). Sporogonie de Plasmodium agamae chez Culicoides nubeculosus au laboratoire. I. Experimentation et description du cycle. Protistologica 19, 537–41.Google Scholar
Pianka, E. R. (1986). Ecology and Natural History of Desert Lizards. Princeton: Princeton University Press.CrossRefGoogle Scholar
Price, P. W. (1980). Evolutionary Biology of Parasites. Princeton: Princeton University Press.Google Scholar
Rand, A. S., Guerrero, S. & Andrews, R. M. (1983). The ecological effects of malaria on the lizard Anolis limifrons, Barro Colorado Island, Panama. In Advances in Herpetology and Evolutionary Biology (ed. Rhodin, A. G. J. & Mivata, K.), pp. 455–71. Cambridge, MA: Harvard University Press.Google Scholar
Read, A. F. (1987). Comparative evidence supports the Hamilton and Zuk hypothesis on parasites and sexual selection. Nature, London 327, 68–70.Google Scholar
Ressel, S. & Schall, J. J. (1989). Parasites and showy males: malarial infection and color variation in fence lizards. Oecologia 78, 158–64.Google Scholar
Russell, P. F., West, L. S., Manwell, R. & Macdonald, C. (1963). Practical Malariology, 2nd edn.London: Oxford University Press.Google Scholar
Ruth, S. B. (1977). A comparison of the demography and female reproduction in sympatric western fence lizards (Sceloporus occidentalis) and sagebrush lizards (Sceloporus graciosus) on Mount Diablo, California. Thesis, University of California at Berkeley.Google Scholar
Schall, J. J. (1977). Thermal ecology of five sympatric Cnemidophorus. Herpetologica 33, 261–72.Google Scholar
Schall, J. J. (1978). Reproductive strategies in sympatric whiptail lizards, Cnemidophorus: two parthenogenetic and three bisexual species. Copeia 1978, 108–16.CrossRefGoogle Scholar
Schall, J. J. (1983 a). Lizard malaria: parasite-host ecology. In Lizard Ecology (ed. Huey, R. B., Pianka, E. R. & Schoener, T. W.), pp. 84–100. Cambridge, MA: Harvard University Press.Google Scholar
Schall, J. J. (1983 b). Lizard malaria: cost to vertebrate host's reproductive success. Parasitology 87, 1–6.Google Scholar
Schall, J. J. (1983 c). Small clutch size in a tropical whiptail lizard (Cnemidophorus arubensis). Journal of Herpetology 17, 406–8.Google Scholar
Schall, J. J. (1986). Prevalence and virulence of a haemogregarine parasite of the Aruban whiptail lizard, Cnemidophorus arubensis. Journal of Herpetology 20, 318–24.Google Scholar
Schall, J. J., Bennett, A. F. & Putnam, R. W. (1982). Lizards infected with malaria: physiological and behavioral consequences. Science 217, 1057–9.CrossRefGoogle ScholarPubMed
Schall, J. J. & Dearing, M. D. (1987). Malarial parasitism and male competition for mates in the western fence lizard, Sceloporus occidentalis. Qecologia 73, 389–92.Google Scholar
Schall, J. J. & Sarni, C. A. (1987). Malarial parasitism and the behavior of the lizard, Sceloporus occidentalis. Copeia 1987, 84–93.CrossRefGoogle Scholar
Scorza, J. V. (1971). Anaemia in lizard malaria infections. Parasitologia 13, 391–405.Google Scholar
Seed, T. M. & Manwell, R. D. (1977). Plasmodia of birds. In Parasitic Protozoa, Vol. 3 (ed. Kreier, J. P.), pp. 311–57. New York: Academic Press.Google Scholar
Stehbens, W. E. & Johnston, M. R. L. (1966). The viral nature of Pirhemocyton tarentolae. Journal of Ultrastructure Research 15, 543–54.CrossRefGoogle ScholarPubMed
Swellengrebel, N. H. (1940). The efficient parasite. Proceedings of the Third International Congress of Microbiology 3, 119–127. Baltimore: Waverly Press.Google Scholar
Sypek, J. & Borysenko, M. (1988). Reptiles. In Vertebrate Blood Cells (ed. Rowley, A. F. & Ratcliffe, N. A.), pp. 211–56. Cambridge: Cambridge University Press.Google Scholar
Telford, S. R. (1971). Parasitic diseases of reptiles. Journal of the American Veterinary Medical Association 158, 1644–52.Google Scholar
Telford, S. R. (1972). The course of infection of Japanese saurian malaria (Plasmodium sasai, Telford & Ball) in natural and experimental hosts. The Japanese Journal of Experimental Medicine 42, 1–21.Google Scholar
Telford, S. R. (1984). Haemoparasites of reptiles. In Diseases of Amphibians and Reptiles (ed. Hoff, C. L., Frye, F. L. & Jacobson, E. R.), pp. 385–517. New York: Plenum.Google Scholar
Theiler, M. (1930). Special protozoological studies of the blood. In The African Republic of Liberia and the Belgian Congo (ed. Strong, R. P.), pp. 490–8. Cambridge, MA: Harvard University Press.Google Scholar
Thompson, P. E. & Huff, C. G. (1944). A saurian malarial parasite, Plasmodium mexicanum, n.sp., with both elongatum and gallinaceum-types of exoerythrocytic stages. Journal of Infectious Diseases 74, 48–67.Google Scholar
Thompson, P. E. & Winder, V. (1947). Analysis of saurian malarial infections as influenced by temperature. Journal of Infectious Diseases 81, 68–79.Google Scholar
Ward, P. I. (1988). Sexual dichromatism and parasitism in British and Irish freshwater fish. Animal Behavior 36, 1210–15.Google Scholar
Weiss, L. (1983). Hematopoietic tissue in malaria: facilitation of erythrocytic cycling by bone marrow in Plasmodium berghei infected mice. Journal of Parasitology 69, 307–18.Google Scholar
Wenyon, C. M. (1909). Report of travelling pathologist and protozoologist. In Third Report, Weilcome Research Laboratory (ed. Balfour, A.), pp. 146–50. London: Tindall and Cox.Google Scholar
Williams, G. C. (1966). Adaptation and Natural Selection. Princeton: Princeton University Press.Google Scholar
Zahavi, A. (1975). Mate selection — a selection for a handicap. Journal of Theoretical Biology 53, 205–14.Google Scholar
Bakker, Zinderen E. M. V. (1978). Quaternary vegetation changes in southern Africa. In Biogeography and Ecology of Southern Africa (ed. Werger, M. J. A.), pp. 131–70. The Hague: Junk.Google Scholar
Zuckerman, A., Spira, D. T. & Ron, N. (1973). A quantitative study of phagocytosis in the spleen of rats infected with Plasmodium berghei. In Dynamic Aspects of Host-Parasite Relationships, Vol. 1 (ed. Zuckerman, A. & Weiss, D. W.), pp. 79–115. New York: Academic Press.Google Scholar
Zuk, M. (1990). Parasites and bright birds: new data and a new prediction. In Ecology, Behaviour and Evolution of Bird—Parasite Interactions (ed. Loye, J. E., Van Riper, C. & Zuk, M.). London: Oxford University Press (in the Press).Google Scholar