Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-28T00:22:19.791Z Has data issue: false hasContentIssue false

Microsatellite loci over a thirty-three year period for a malaria parasite (Plasmodium mexicanum): bottleneck in effective population size and effect on allele frequencies

Published online by Cambridge University Press:  05 September 2012

J. J. SCHALL*
Affiliation:
Department of Biology, University of Vermont, Burlington, VT 05405, USA
K. M. ST. DENIS
Affiliation:
Department of Biology, University of Vermont, Burlington, VT 05405, USA
*
*Corresponding author: Tel: +802 656 0448. Fax: +802 656 2914. E-mail: [email protected]

Summary

Changes in population allele frequencies may be driven by several forces, including selection and drift, and are revealed only by sampling over many generations. Such studies, however, are rare for protist parasites. Microsatellite allele frequencies for 4 loci were followed in a population of Plasmodium mexicanum, a malaria parasite of lizards in California USA at 1 site from 1978 to 2010. Rapid turnover of the lizards indicates the parasite was studied for a minimum of 33 transmission cycles and possibly twice that number. Sample sizes ranged from 841 to 956 scored parasite clones per locus. DNA was extracted from frozen dried blood and blood removed from stained blood smears from the earliest years, and a verification study demonstrated DNA from the blood smears provided valid genetic data. Parasite prevalence and effective population size (Ne) dropped after 2000, remaining lower for the next decade. For 2 loci, allele frequencies appeared stable for the first 2 decades of the study, but changed more rapidly after the decline in prevalence. Allele frequencies changed more gradually for the other 2 loci. Genetic drift could account for changes in allele frequencies, especially after the drop in prevalence and Ne, but the force of selection could also have driven the observed patterns.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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

REFERENCES

Abdel-Muhsin, A. A., Mackinnon, M. J., Awadalle, P., Alli, E., Suleiman, S., Ahmed, S., Walliker, D. and Babiker, H. A. (2003). Local differentiation in Plasmodium falciparum drug resistance genes in Sudan. Parasitology 126, 391400.CrossRefGoogle ScholarPubMed
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 loci reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Molecular Biology and Evolution 17, 14671482.CrossRefGoogle ScholarPubMed
Bonizzoni, M., Afrane, Y., Baliraine, F. N., Amenya, D. A., Githeko, A. K., Yan, G. and Githeko, A. K. (2009). Infection Genetic structure of Plasmodium falciparum populations between lowland and highland sites and antimalarial drug resistance in Western Kenya. Genetics and Evolution 9, 806812.CrossRefGoogle ScholarPubMed
Bromwich, C. R. and Schall, J. J. (1986). Infection dynamics of Plasmodium mexicanum, a malarial parasite of lizards. Ecology 67, 12271235.CrossRefGoogle Scholar
Conway, D. J. C., Machado, R. L., Singh, B., Dessert, P., Mikes, Z. S., Povoa, M. M., Oduola, A. and Roper, C. (2001). Extreme geographical fixation of variation in the Plasmodium falciparum gamete surface protein gene Pfs48/45 compared with microsatellite loci. Molecular and Biochemical Parasitology 115, 145156.CrossRefGoogle ScholarPubMed
Eisen, R. J. (2001). Absence of measurable malaria-induced mortality in western fence lizards (Sceloporus occidentalis) in nature: a four year study of annual and over-winter mortality. Oecologia 127, 586589.CrossRefGoogle 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, 12181226.CrossRefGoogle ScholarPubMed
Ford, A. F. and Schall, J. J. (2011). Relative clonal proportions over time in mixed-genotype infections of the lizard malaria parasite P. mexicanum. International Journal for Parasitology 41, 731738.CrossRefGoogle Scholar
Ford, A. F., Vardo-Zalik, A. M., Schall, J. J. (2010). Relative clonal density of two malaria parasites, Plasmodium falciparum and P. mexicanum, in mixed genotype infections: validation of a technique using microsatellite markers. Journal of Parasitology 96, 908913.CrossRefGoogle Scholar
Freeman, S. and Herron, J. C. (2007). Evolutionary Analysis, 4th Edn.Pearson Education, Upper Saddle River, NJ, USA.Google Scholar
Fricke, J. M., Vardo-Zalik, A. M. and Schall, J. J. (2010). Geographic genetic differentiation of a malaria parasite, Plasmodium mexicanum, and it lizard host, Sceloporus occidentalis. Journal of Parasitology 96, 308313.CrossRefGoogle ScholarPubMed
Garza, J. C. and Williamson, E. G. (2001). Detection of reduction in population size using data from microsatellite loci. Molecular Ecology 10, 305318.CrossRefGoogle ScholarPubMed
Ghedin, E., Sengamalay, N. A., Shumway, M., Zaborsky, J., Feldblyum, T., Subbu, V., Spiro, D. J., Sitz, J., Koo, H., Bolotov, P., Dernovoy, D., Tatusova, T., Bao, Y., St. George, K., Taylor, J.Lipman, D. J., Fraser, C. M., Taubenberger, J. K. and Salzberg, S. L. (2005). Large-scale sequencing of human influenza reveals the dynamic nature of viral genome evolution. Nature, London 437, 11621166.CrossRefGoogle ScholarPubMed
Haldane, J. B. S. (1932). The Causes of Evolution. Longmans, Green, London, UK.Google Scholar
Hastings, I. M., Nsanzabana, C. and Smith, T. A. (2010). A comparison of methods to detect and quantify the markers of antimalarial drug resistance. American Journal of Tropical Medicine and Hygiene 83, 489495.CrossRefGoogle ScholarPubMed
Havryliuk, T., Orjuela-Sanchez, P. and Ferreira, M. U. (2008). Plasmodium vivax: Microsatellite analysis of multiple-clone infections. Experimental Parasitology 120, 330336.CrossRefGoogle ScholarPubMed
Hutchinson, W. F., van Oosterhout, C., Rogers, S. I. and Carvalho, G. R. (2003). Temporal analysis of archived samples indicates marked genetic changes in declining North Sea cod (Gadus morhua). Proceedings of the Royal Society of London, B 270, 21252132.CrossRefGoogle ScholarPubMed
Johnson, J. A., Bellinger, M. R., Toepfer, J. E. and Dunn, P. (2004). Temporal changes in allele frequencies and low effective population size in greater prairie-chickens. Molecular Ecology 13, 26172630.CrossRefGoogle ScholarPubMed
Martinsen, E. M., Perkins, S. L. and Schall, J. J. (2008). A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): Evolution of life-history traits and host switches. Molecular Phylogenetics and Evolution 47, 261273.CrossRefGoogle ScholarPubMed
May, R. M. (1991). The dynamics and genetics of host-parasite associations. In Parasite-Host Associations, Coexistence or conflict? (ed. Toft, C. A., Aeschlimann, A. and Bolis, L.), pp. 102128. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Nair, S., Williams, J. T., Brockman, A., Paiphun, L., Mayxay, M., Newton, P. N., Guthmann, J.-P., Smithuis, F. M., Hien, T. T., White, N. J., Nosten, F. and Anderson, T. J. C. (2003). A selective sweep driven by pyrimethamine treatment in Southeast Asian malaria parasites. Molecular Biology and Evolution 20, 15261536.CrossRefGoogle ScholarPubMed
Neal, A. T. and Schall, J. J. (2010). Gametocyte sex ratio in single-clone infections of the malaria parasite Plasmodium mexicanum. Parasitology 137, 18511859.CrossRefGoogle ScholarPubMed
Orjuela-Sanchez, P., da Silva-Nunes, M., da Silva, N. S., Scopel, K. K. G., Gonçalves, R. M., Malafronte, R. S. and Ferreira, M. U. (2009). Population dynamics of genetically diverse Plasmodum falciparum lineages: community-based prospective study in rural Amazonia. Parasitology 136, 10971105.CrossRefGoogle Scholar
Peakall, R. and Smouse, P. E. (2006). genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288295.CrossRefGoogle 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, 15871590.CrossRefGoogle Scholar
Price, P. W. (1980). Evolutionary Biology of Parasites. Princeton University Press, Princeton, NJ, USA.Google ScholarPubMed
Provine, W. B. (1971). The Origins of Theoretical Population Genetics. The University of Chicago Press, Chicago, IL, USA.Google Scholar
Rossetto, M., Kooyman, R., Sherwin, W. and Jones, R. (2008). Dispersal limitation, rather than bottlenecks or habitat specificity, can restrict the distribution of rare and endangered rainforest trees. American Journal of Botany 95, 321329.CrossRefGoogle ScholarPubMed
Schall, J. J. (1996). Malarial parasites of lizards: Diversity and ecology. Advances in Parasitology 37, 255333.CrossRefGoogle ScholarPubMed
Schall, J. J. and Vardo, A. M. (2007). Identification of microsatellite loci in Plasmodium mexicanum, a lizard malaria parasite that infects nucleated erythrocytes. Molecular Ecology Notes 7, 227229.CrossRefGoogle Scholar
Selkoe, K. A. and Toonen, R. J. (2006). Microsatellites for ecologists: a practical guide to using and evaluating microsatellite loci. Ecology Letters 9, 615629.CrossRefGoogle Scholar
Sherwin, W. B., Jabot, F., Rush, E. and Rossetto, M. (2006). Measurement of biological information with applications from genes to landscapes. Molecular Ecology 15, 28572869.CrossRefGoogle ScholarPubMed
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, 27122720.CrossRefGoogle ScholarPubMed
Vardo-Zalik, A. M., Ford, A. F. and Schall, J. J. (2009). Detecting number of clones, and their relative abundance, of a malaria parasite (Plasmodium mexicanum) infecting its vertebrate host. Parasitology Research 105, 209215.CrossRefGoogle ScholarPubMed
Vardo-Zalik, A. M. and Schall, J. J. (2008). Clonal diversity within infections and virulence of a malaria parasite, Plasmodium mexicanum. Parasitology 135, 13631372.CrossRefGoogle ScholarPubMed
Vardo-Zalik, A. M. and Schall, J. J. (2009). Clonal diversity alters the infection dynamics of a malaria parasite (Plasmodium mexicanum) in its vertebrate host. Ecology 90, 529536.CrossRefGoogle ScholarPubMed
Wang, J. (2005). Estimation of effective population sizes from data on genetic markers. Philosophical Proceedings of the Royal Society of London, B 360, 13951409.Google ScholarPubMed
Wright, S. (1977). Evolution and the Genetics of Populations, Vol. 2. Experimental Results and Evolutionary Deductions. University of Chicago Press, Chicago, IL, USA.Google Scholar
Zhong, D., Afrane, Y., Githeko, A., Yang, Z., Cui, L., Menge, D. M., Temu, E. A. and Yan, G. (2007). Plasmodium falciparum genetic diversity in western Kenya highlands. American Journal of Tropical Medicine and Hygiene 77, 10431050.CrossRefGoogle ScholarPubMed