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Clonal diversity within infections and the virulence of a malaria parasite, Plasmodium mexicanum

Published online by Cambridge University Press:  21 October 2008

A. M. Vardo-ZALIK  and
J. J. Schall
A. M. Vardo-ZALIK*
Affiliation:
University of Vermont, Burlington, Vermont 05405, USA
J. J. Schall
Affiliation:
University of Vermont, Burlington, Vermont 05405, USA
*
*Corresponding author: Tel: +949 824 0249. Fax: +949 824 0249. E-mail: [email protected]
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Summary

Both verbal and mathematical models of parasite virulence predict that genetic diversity of microparasite infections will influence the level of costs suffered by the host. We tested this idea by manipulating the number of co-existing clones of Plasmodium mexicanum in its natural vertebrate host, the fence lizard Sceloporus occidentalis. We established replicate infections of P. mexicanum made up of 1, 2, 3, or >3 clones (scored using 3 microsatellite loci) to observe the influence of clone number on several measures of parasite virulence. Clonal diversity did not affect body growth or production of immature erythrocytes. Blood haemoglobin concentration was highest for the most genetically complex infections (equal to that of non-infected lizards), and blood glucose levels and rate of blood clotting was highest for the most diverse infections (with greater glucose and more rapid clotting than non-infected animals). Neither specific clones nor parasitaemia were associated with virulence. In this first experiment that manipulated the clonal diversity of a natural Plasmodium-host system, the cost of infection with 1 or 2 clones of P. mexicanum was similar to that previously reported for infected lizards, but the most complex infections had either no cost or could be beneficial for the host.

Keywords

malariaPlasmodium mexicanumvirulenceclonal diversitymicrosatellites
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 12 , October 2008 , pp. 1363 - 1372
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Anderson, T. J. C., Haubold, B., Williams, J. T., Estrada-Franco, J. G., Richardson, L., Mollinedo, R., Bockarie, M., Mokili, J., Mharakurwa, S., French, N., Whitworth, J., Velez, I. D., Brockman, A. H., Nosten, F., Ferreira, M. U. and Day, K. P. (2000). Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Molecular Biology and Evolution 17, 1467–1482.CrossRefGoogle ScholarPubMed
Bogreau, H., Renaud, F. O., Bouchiba, H., Durand, P., Assi, S. B., Henry, M. C., Garnotel, E., Pradines, B., Fusai, T., Wade, B., Adehossi, E., Parola, P., Ali Kamil, M., Puijalon, O. and Rogier, C. (2006). Genetic diversity and structure of African Plasmodium falciparum populations in urban and rural areas. American Journal of Tropical Medicine and Hygiene 74, 953–959.CrossRefGoogle ScholarPubMed
Bromwich, C. R. and Schall, J. J. (1986). Infection dynamics of Plasmodium mexicanum, a malarial parasite of lizards. Ecology 67, 1227–1235. doi: 10.2307/1938678CrossRefGoogle Scholar
Bruce, M., Macheso, A., Galinski, M. and Barnwell, J. (2007). Characterization and application of multiple genetic markers for Plasmodium malariae. Parasitology 134, 637–650. doi: 10.1017/S0031182006001958CrossRefGoogle ScholarPubMed
Bull, J. J. (1994). Perspective – virulence. Evolution 48, 1423–1437.Google ScholarPubMed
Chandavar, V. R. and Naik, P. R. (2004). Variation in plasma glucose and pancreatic beta cells in the turtle, Lissemys punctata (order: Chelonia; family: Trionychidae). Acta Zoologica 85, 113–118. doi:10.1111/j.0001-7272.2004.00163.xCrossRefGoogle Scholar
Cui, L. W., Mascorro, C. N., Fan, Q., Rzomp, K. A., Khuntirat, B., Zhou, G., Chen, H., Yan, G. Y. and Sattabongkot, J. (2003). Genetic diversity and multiple infections of Plasmodium vivax malaria in western Thailand. American Journal of Tropical Medicine and Hygiene 68, 613–619.CrossRefGoogle ScholarPubMed
de Roode, J. C., Culleton, R., Cheesman, S. J., Carter, R. and Read, A. F. (2004). Host heterogeneity is a determinant of competitive exclusion or coexistence in genetically diverse malaria infections. Proceedings of the Royal Society of London, B 271, 1073–1080. doi: 10.1098/rspb.2004.2695CrossRefGoogle ScholarPubMed
de Roode, J. C., Helinski, M. E. H., Anwar, M. A. and Read, A. F. (2005 a). Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. American Naturalist 166, 531–542. doi: 10.1086/491659CrossRefGoogle ScholarPubMed
de Roode, J. C., Pansini, R., Cheesman, S. J., Helinski, M. E. H., Huijben, S., Wargo, A. R., Bell, A. S., Chan, B. H. K., Walliker, D. and Read, A. F. (2005 b). Virulence and competitive ability in genetically diverse malaria infections. Proceedings of the National Academy of Sciences, USA 102, 7624–7628. doi: 10.1073/pnas.0500078102CrossRefGoogle ScholarPubMed
de Roode, J. C., Read, A. F., Chan, B. H. K. and Mackinnon, M. J. (2003). Rodent malaria parasites suffer from the presence of conspecific clones in three-clone Plasmodium chabaudi infections. Parasitology 127, 411–418. doi:10.1017/S0031182003004001CrossRefGoogle ScholarPubMed
Dunlap, K. D. and Schall, J. J. (1995). Hormonal alterations and reproductive inhibition in male fence lizards (Sceloporus occidentalis) infected with the malarial parasite Plasmodium mexicanum. Physiological Zoology 68, 608–621.CrossRefGoogle Scholar
Eisen, R. J. (2001). Absence of measurable malaria-induced mortality in western fence lizards (Sceloporus occidentalis) in nature: a 4-year study of annual and over-winter mortality. Oecologia 127, 586–589. doi: 10.1007/s004420000626CrossRefGoogle ScholarPubMed
Eisen, R. J. and Schall, J. J. (1997). Comparing foraging success in submissive malaria-infected and territorial noninfected fence lizards (Sceloporus occidentalis). Journal of Herpetology 31, 147–149.CrossRefGoogle Scholar
Eisen, R. J. and Schall, J. J. (2000). Life history of a malaria parasite (Plasmodium mexicanum): Assessment of independent traits and origin of variation. Proceedings of the Royal Society of London, B 26, 793–799. doi:10.1098/rspb.2000.1073CrossRefGoogle Scholar
Ewald, P. W. (1994). Evolution of Infectious Disease. Oxford University Press, New York, USA.CrossRefGoogle Scholar
Ewald, P. W. (2004). Evolution of virulence. Infectious Disease Clinics of North America 18, 1–15.CrossRefGoogle ScholarPubMed
Felger, I., Smith, T., Edoh, T., Kitua, A., Alonso, P., Tanner, M. and Beck, H. P. (1999). Epidemiology of multiple Plasmodium falciparum infections – 6. Multiple Plasmodium falciparum infections in Tanzanian infants. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, S29–S34. doi:10.1016/S0035-9203(99)90324-3CrossRefGoogle Scholar
Ferreira, M. U., Karunaweera, N. D., Da Silva-Nunes, M., Da Silva, N. S., Wirth, D. F. and Hartl, D. L. (2007). Population structure and transmission dynamics of Plasmodium vivax in rural amazonia. Journal of Infectious Diseases 195, 1218–1226. doi:10.1086/512685CrossRefGoogle ScholarPubMed
Ferreira, M. U., Nair, S., Hyunh, T. V., Kawamoto, F. and Anderson, T. J. C. (2002). Microsatellite characterization of Plasmodium falciparum from cerebral and uncomplicated malaria patients in Southern Vietnam. Journal of Clinical Microbiology 40, 1854–1857. doi: 10.1128/JCM.40.5.1854-1857CrossRefGoogle ScholarPubMed
Fialho, R. F. and Schall, J. J. (1995). Thermal ecology of a malarial parasite and its insect vector: consequences for the parasite's transmission success. Journal of Animal Ecology 64, 553–562. doi: 10.2307/5799CrossRefGoogle Scholar
Frank, S. A. (1996). Models of parasite virulence. Quarterly Review of Biology 71, 37–78. doi: 10.1086/419267.CrossRefGoogle ScholarPubMed
Ghosh, K. and Shetty, S. (2008). Blood coagulation in falciparum malaria- a review. Parasitological Research 102, 571–576. doi:10.1007/s00436-007-0832-0.CrossRefGoogle ScholarPubMed
Gotelli, N. J. and Ellison, A. M. (2004). A Primer of Ecological Statistics. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Gupta, S., Hill, A. V. S., Kwiatkowski, D., Greenwood, A. M., Greenwood, B. M. and Day, K. P. (1994). Parasite virulence and disease patterns in Plasmodium falciparum malaria. Proceedings of the National Academy of Sciences, USA 91, 3715–3719. doi: 10.1073/pnas.91.9.3715CrossRefGoogle ScholarPubMed
Imwong, M., Sudimack, D., Pukrittayakamee, S., Osorio, L., Carlton, J. M., Day, N. P. J., White, N. J. and Anderson, T. J. C. (2006). Microsatellite variation, repeat array length, and population history of Plasmodium vivax. Molecular Biology and Evolution 23, 1116–1018. doi: 10.1093/molber/msj116CrossRefGoogle ScholarPubMed
Khanna, S. S. and Kumar, S. (1975). Blood glucose in the common Indian sand lizard Uromastix hardwicki. Copeia 4, 767–771.CrossRefGoogle Scholar
Leclerc, M. C., Durand, P., De Meeus, T., Robert, V. and Renaud, F. (2002). Genetic diversity and population structure of Plasmodium falciparum isolates from Dakar, Senegal, investigated from microsatellite and antigen determinant loci. Microbes and Infection 4, 685–692. doi:10.1016/S1286-4579(02)01587-3CrossRefGoogle ScholarPubMed
Mackinnon, M., Gaffney, D. and Read, A. (2002). Virulence in rodent malaria: host genotype by parasite genotype interactions. Infection, Genetics and Evolution 1, 287–296. doi:10.1016/S1567-1348(02)00039-4CrossRefGoogle ScholarPubMed
Mackinnon, M. J. and Read, A. F. (1999). Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 53, 689–703. doi: 10.2307/2640710CrossRefGoogle ScholarPubMed
Mackinnon, M. J. and Read, A. F. (2003). The effects of host immunity on virulence-transmissibility relationships in the rodent malaria parasite Plasmodium chabaudi. Parasitology 126, 103–112. doi:10.1017/S003118200200272XCrossRefGoogle ScholarPubMed
Mackinnon, M. J. and Read, A. F. (2004). Virulence in malaria: an evolutionary viewpoint. Philosophical Transactions of the Royal Society of London, B 359, 965–986. doi: 10.1098/rstb.2003.1414CrossRefGoogle ScholarPubMed
May, R. M. and Nowak, M. A. (1995). Coinfection and the evolution of parasite virulence. Proceedings of the Royal Society of London, B 261, 209–215.Google ScholarPubMed
Mehta, M., Sonawat, H. M. and Sharma, S. (2005). Malaria parasite-infected erythrocytes inhibit glucose utilization in uninfected red cells. FEBS Letters 579, 6151–6158. doi:10.1016/j.febslet.2005.09.088CrossRefGoogle ScholarPubMed
Müller, D. A., Charlwood, J. D., Felger, I., Ferreira, C., do Rosario, V. and Smith, T. (2001). Prospective risk of morbidity in relation to multiplicity of infection with Plasmodium falciparum in São Tomé. Acta Tropica 78, 155–162. doi:10.1016/S0001-706X(01)00067-5CrossRefGoogle ScholarPubMed
Nowak, M. A. and May, R. M. (1994). Superinfection and the evolution of parasite virulence. Proceedings of the Royal Society of London, B 255, 81–89.Google ScholarPubMed
Nwakanma, D., Kheir, A., Sowa, M., Dunyo, S., Jawara, M., Pinder, M., Milligan, P., Walliker, D. and Babiker, H. A. (2008). High gametocyte complexity and mosquito infectivity of Plasmodium falciparum in the Gambia. International Journal for Parasitology 38, 219–227. doi:10.1016/j.ijpara.2007.07.003.CrossRefGoogle ScholarPubMed
Ofosu-Okyere, A., Mackinnon, M. J., Sowa, M. P. K., Koram, K. A., Nkumah, F., Osei, Y. D., Hill, W. G., Wilson, M. D. and Arnot, D. E. (2001). Novel Plasmodium falciparum clones and rising clone multiplicities are associated with the increase in malaria morbidity in Ghanaian children during the transition into the high transmission season. Parasitology 123, 113–123. doi:10.1017/S0031182001008162CrossRefGoogle ScholarPubMed
Osgood, S. M., Eisen, R. J., Wargo, A. R. and Schall, J. J. (2003). Manipulation of the vertebrate host's testosterone does not affect gametocyte sex ratio of a malaria parasite. Journal of Parasitology 89, 190–192. doi: 10.1645/0022-3395(2003)089 [0190:MOTVHT] 2.0.CO;2CrossRefGoogle Scholar
Osgood, S. M. and Schall, J. J. (2003). Gametocyte sex ratio of a malaria parasite: response to experimental manipulation of parasite clonal diversity. Parasitology 128, 23–29. doi:10.1017/S0031182003004207CrossRefGoogle Scholar
Perkins, S. L., Osgood, S. M. and Schall, J. J. (1998). Use of PCR for detection of subpatent infections of lizard malaria: implications for epizootiology. Molecular Ecology 7, 1587–1590. doi:10.1046/j.1365-294x.1998.00496.xCrossRefGoogle Scholar
Read, A. F. and Taylor, L. H. (2001). The ecology of genetically diverse infections. Science 292, 1099–1102. doi: 10.1126/science.1059410CrossRefGoogle ScholarPubMed
Ressel, S. and Schall, J. J. (1989). Parasites and showy males: malarial infection and color variation in fence lizards. Oecologia 78, 158–164. doi:10.1007/BF00377151CrossRefGoogle ScholarPubMed
Schall, J. J. (1983). Lizard malaria – cost to vertebrate hosts reproductive success. Parasitology 87, 1–6.CrossRefGoogle Scholar
Schall, J. J. (1990 a). The ecology of lizard malaria. Parasitology Today 6, 264–269.CrossRefGoogle ScholarPubMed
Schall, J. J. (1990 b). Virulence of lizard malaria: the evolutionary ecology of an ancient parasite host association. Parasitology 100, S35–S52.CrossRefGoogle ScholarPubMed
Schall, J. J. (1996). Malarial parasites of lizards: diversity and ecology. Advances in Parasitology 37, 255–333.CrossRefGoogle ScholarPubMed
Schall, J. J. (2002). Parasite virulence. In The Behavioural Ecology of Parasites (ed. Lewis, E., Campbell, J. and Sukhdeo, M.) pp. 283–313. CAB International, Oxon, UK.CrossRefGoogle Scholar
Schall, J. J., Bennett, A. F. and Putnam, R. W. (1982). Lizards infected with malaria: physiological and behavioral consequences. Science 217, 1057–1059. doi:10.1126/science.7112113CrossRefGoogle ScholarPubMed
Schall, J. J. and Marghoob, A. B. (1995). Prevalence of a malarial parasite over time and space: Plasmodium mexicanum in its vertebrate host, the western fence lizard, Sceloporus occidentalis. Journal of Animal Ecology 64, 177–185.CrossRefGoogle Scholar
Schall, J. J. and Smith, T. C. (2006). Detection of a malaria parasite (Plasmodium mexicanum) in ectoparasites (mites and ticks), and possible significance for transmission. Journal of Parasitology 92, 413–415. doi: 10.1645/GE-688R.1CrossRefGoogle ScholarPubMed
Schall, J. J. and Vardo, A. M. (2007). Identification of microsatellite markers in Plasmodium mexicanum, a lizard malaria parasite that infects nucleated erythrocytes. Molecular Ecology Notes 7, 227–229. doi: 10.1111/j.1471-8286.2006.01528.xCrossRefGoogle Scholar
Sheldon, B. C. and Verhulst, S. (1996). Ecological immunology: Costly parasite defenses and trade-offs in evolutionary ecology. Trends in Ecology & Evolution 11, 317–321. doi:10.1016/0169-5347(96)10039-2.CrossRefGoogle ScholarPubMed
Smith, T., Felger, I., Tanner, M. and Beck, H. P. (1999). The epidemiology of multiple Plasmodium falciparum infections – 11. Premunition in Plasmodium falciparum infection: insights from the epidemiology of multiple infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, S59–S64. doi: 10.1016/S0035-9203(99)90329-2.CrossRefGoogle Scholar
Tanner, M., Beck, H. P., Felger, I. and Smith, T. (1999). The epidemiology of multiple Plasmodium falciparum infections – 1. General introduction. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, S1–S2. doi:10.1016/S0035-9203(99)90319-XCrossRefGoogle ScholarPubMed
Taylor, L. H., Mackinnon, M. J. and Read, A. F. (1998). Virulence of mixed-clone and single-clone infections of the rodent malaria Plasmodium chabaudi. Evolution 52, 583–591. doi: 10.2307/2411092CrossRefGoogle ScholarPubMed
Valkiunas, G., Anwar, A. M., Atkinson, C. T., Greiner, E. C., Paperna, I. and Peirce, M. A. (2005). What distinguishes malaria parasites from other pigmented haemosporidians? Trends in Parasitology 21, 357–358. doi:10.1016/j.pt.2005.06.005CrossRefGoogle ScholarPubMed
Van Baalen, M. and Sabelis, M. W. (1995). The dynamics of multiple infection and the evolution of virulence. American Naturalist 146, 881–910.CrossRefGoogle Scholar
Vardo, A. M., Kaufhold, K. D. and Schall, J. J. (2007). Experimental test for premunition in a lizard malaria parasite (Plasmodium mexicanum). Journal of Parasitology 93, 280–282. doi: 10.1645/GE-1005R.1CrossRefGoogle Scholar
Vardo, A. M. and Schall, J. J. (2007). Clonal diversity of a lizard malaria parasite, Plasmodium mexicanum, in its vertebrate host, the western fence lizard: role of variation in transmission intensity over time and space. Molecular Ecology 16, 2712–2720. doi: 10.1111/j.1365-294X.2007.03355.xCrossRefGoogle ScholarPubMed
Vardo, A. M., Wargo, A. R. and Schall, J. J. (2005). PCR detection of lizard malaria parasites: Prevalence of Plasmodium infections with low-level parasitemia differs by site and season. Journal of Parasitology 91, 1509–1511. doi: 10.1645/GE-589R.1CrossRefGoogle ScholarPubMed
Vardo-Zalik, A. M. and Schall, J. J. (2008). Clonal diversity alters the infection dynamics of a malaria parasite (Plasmodium mexicanum) within its vertebrate host. Ecology (in the Press).Google Scholar
Voituron, Y., Storey, J., Grenot, C. and Storey, K. (2002). Freezing survival, body ice and blood composition of the freeze-tolerant European common lizard, Lacerta vivipara. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 172, 71–76. doi: 10.1007/s003600100228Google ScholarPubMed