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

Parasitology

Volumn 135, Issue 12, 2008, Pages 1363-1372

  Vardo Zalik, A M ^a   Schall, J J ^a  

^a UNIVERSITY OF VERMONT   (United States)

Author keywords

Clonal diversity; Malaria; Microsatellites; Plasmodium mexicanum; Virulence

Indexed keywords

GLUCOSE; HEMOGLOBIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD CLOTTING; CLONAL SPECIES; CLONAL VARIATION; CONTROLLED STUDY; GLUCOSE BLOOD LEVEL; HEMOGLOBIN BLOOD LEVEL; HOST PARASITE INTERACTION; LIZARD; MATHEMATICAL MODEL; MICROBIAL DIVERSITY; NONHUMAN; PARASITE VIRULENCE; PARASITEMIA; PLASMODIUM; PLASMODIUM MEXICANUM; PRIORITY JOURNAL; SCLELOPORUS OCCIDENTALIS;

ANIMALS; GENETIC VARIATION; LIZARDS; MALE; PARASITEMIA; PLASMODIUM; VIRULENCE;

ANIMALIA; PLASMODIUM MEXICANUM; SCELOPORUS OCCIDENTALIS; SCELOPORUS UNDULATUS; SQUAMATA; VERTEBRATA;

EID: 54349120072     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182008004964     Document Type: Article

References (63)

1. 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.
2. 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.
3. Bromwich, C. R. and Schall, J. J. (1986). Infection dynamics of Plasmodium mexicanum, a malarial parasite of lizards. Ecology 67, 1227-1235. doi: 10.2307/1938678
4. 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/S0031182006001958
5. Bull, J. J. (1994). Perspective - virulence. Evolution 48, 1423-1437.
6. 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.x
7. 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.
8. 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. 2695
9. de Roode, J. C., Helinski, M. E. H., Anwar, M. A. and Read, A. F. (2005a). Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. American Naturalist 166, 531-542. doi: 10.1086/491659
10. 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. (2005b). Virulence and competitive ability in genetically diverse malaria infections. Proceedings of the National Academy of Sciences, USA 102, 7624-7628. doi: 10.1073/pnas.0500078102
11. 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/S0031182003004001
12. 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.
13. 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/s004420000626
14. 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.
15. 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.2000.1073
16. Ewald, P. W. (1994). Evolution of Infectious Disease. Oxford University Press, New York, USA.
17. Ewald, P. W. (2004). Evolution of virulence. Infectious Disease Clinics of North America 18, 1-15.
18. 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)90324-3
19. 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:10.1086/512685
20. 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.40.5.1854-1857
21. 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: 10.2307/5799
22. Frank, S. A. (1996). Models of parasite virulence. Quarterly Review of Biology 71, 37-78. doi: 10.1086/419267.
23. 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.
24. Gotelli, N. J. and Ellison, A. M. (2004). A Primer of Ecological Statistics. Sinauer Associates, Sunderland, MA, USA.
25. 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.91.9.3715
26. 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/msj116
27. Khanna, S. S. and Kumar, S. (1975). Blood glucose in the common Indian sand lizard Uromastix hardwicki. Copeia 4, 767-771.
28. 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)01587-3
29. 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)00039-4
30. 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: 10.2307/2640710
31. 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/S003118200200272X
32. 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.2003.1414
33. 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.
34. 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. 088
35. 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) 00067-5
36. 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.
37. 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.
38. 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/S0031182001008162
39. 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;2
40. 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/S0031182003004207
41. 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.x
42. Read, A. F. and Taylor, L. H. (2001). The ecology of genetically diverse infections. Science 292, 1099-1102. doi: 10.1126/science.1059410
43. 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/BF00377151
44. Schall, J. J. (1983). Lizard malaria - cost to vertebrate hosts reproductive success. Parasitology 87, 1-6.
45. Schall, J. J. (1990a). The ecology of lizard malaria. Parasitology Today 6, 264-269.
46. Schall, J. J. (1990b). Virulence of lizard malaria: the evolutionary ecology of an ancient parasite host association. Parasitology 100, S35-S52.
47. Schall, J. J. (1996). Malarial parasites of lizards: diversity and ecology. Advances in Parasitology 37, 255-333.
48. 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.
49. 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.7112113
50. 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.
51. 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.1
52. 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.x
53. 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.
54. 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.
55. 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-X
56. 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: 10.2307/2411092
57. 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.2005.06.005
58. Van Baalen, M. and Sabelis, M. W. (1995). The dynamics of multiple infection and the evolution of virulence. American Naturalist 146, 881-910.
59. 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.1
60. 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.x
61. 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.1
62. 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).
63. 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/s003600100228