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Primary peak and chronic malaria infection levels are correlated in experimentally infected great reed warblers

Published online by Cambridge University Press:  01 May 2012

MUHAMMAD ASGHAR ,
HELENA WESTERDAHL ,
PAVEL ZEHTINDJIEV ,
MIHAELA ILIEVA ,
DENNIS HASSELQUIST  and
STAFFAN BENSCH
MUHAMMAD ASGHAR*
Affiliation:
Department of Biology, Molecular Ecology and Evolution Lab, Lund University, Ecology Building, Sölvegatan 37, 223 62 Lund, Sweden
HELENA WESTERDAHL
Affiliation:
Department of Biology, Molecular Ecology and Evolution Lab, Lund University, Ecology Building, Sölvegatan 37, 223 62 Lund, Sweden
PAVEL ZEHTINDJIEV
Affiliation:
Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113 Sofia, Bulgaria
MIHAELA ILIEVA
Affiliation:
Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113 Sofia, Bulgaria
DENNIS HASSELQUIST
Affiliation:
Department of Biology, Molecular Ecology and Evolution Lab, Lund University, Ecology Building, Sölvegatan 37, 223 62 Lund, Sweden
STAFFAN BENSCH
Affiliation:
Department of Biology, Molecular Ecology and Evolution Lab, Lund University, Ecology Building, Sölvegatan 37, 223 62 Lund, Sweden
*
*Corresponding author: Department of Biology, Molecular Ecology and Evolution Lab, Lund University, Ecology Building, Sölvegatan 37, 223 62 Lund, Sweden. E-mail: [email protected]
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Summary

Malaria parasites often manage to maintain an infection for several months or years in their vertebrate hosts. In humans, rodents and birds, most of the fitness costs associated with malaria infections are in the short initial primary (high parasitaemia) phase of the infection, whereas the chronic phase (low parasitaemia) is more benign to the host. In wild birds, malaria parasites have mainly been studied during the chronic phase of the infection. This is because the initial primary phase of infection is short in duration and infected birds with severe disease symptoms tend to hide in sheltered places and are thus rarely caught and sampled. We therefore wanted to investigate the relationship between the parasitaemia during the primary and chronic phases of the infection using an experimental infection approach. We found a significant positive correlation between parasitaemia in the primary peak and the subsequent chronic phase of infection when we experimentally infected great reed warblers (Acrocephalus arundinaceus) with Plasmodium ashfordi. The reason for this association remains to be understood, but might arise from individual variation in exoerythrocytic parasite reservoirs in hosts, parasite antigenic diversity and/or host genetics. Our results suggest that the chronic phase parasitaemia can be used to qualitatively infer the parasitaemia of the preceding and more severe primary phase, which is a very important finding for studies of avian malaria in wild populations.

Keywords

Acrocephalus arundinaceusPlasmodium ashfordiparasitaemiaprimary infectionschronic infections
Type
Research Article
Information
Parasitology , Volume 139 , Issue 10 , September 2012 , pp. 1246 - 1252
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Asghar, M., Hasselquist, D. and Bensch, S. (2011). Are chronic avian Haemosporidian infections costly in wild birds? Journal of Avian Biology 42, 530–537.CrossRefGoogle Scholar
Atkinson, C. T., Dusek, R. J., Woods, K. L. and Iko, W. M. (2000). Pathogenicity of avian malaria in experimentally infected Hawaii amakihi. Journal of Wildlife Diseases 36, 197–204.CrossRefGoogle ScholarPubMed
Atkinson, C. T. and van Riper, I. (1991). Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus, In Bird–Parasite Interactions: Ecology, Evolution and Behavior. (ed. Loye, J. E. and Zuk, M.), pp. 19–48. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Bejerano, G., Pheasant, M., Makunin, I., Stephen, S., Kent, W., Mattick, J. S. and Haussler, D. (2004). Ultra-conserved elements in the human genome. Science 304, 1321–1325.CrossRefGoogle Scholar
Bell, A. S, de Roode, J. C., Sim, D. and Read, A. F. (2006). Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution 60, 1358–1371.Google ScholarPubMed
Bensch, S., Stjerman, M., Hasselquist, D., Ostman, O., Hansson, B., Westerdahl, H. and Pinheiro, R. T. (2000). Host specificity and avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society of London, B 267, 1583–1589.CrossRefGoogle ScholarPubMed
Bensch, S., Waldenström, J., Jonzén, N., Westerdahl, H., Hansson, B., Sejberg, D. and Hasselquist, D. (2007). Temporal dynamics and diversity of avian malaria parasites in a single host species. Journal of Animal Ecology 76, 112–122.CrossRefGoogle Scholar
Calderaro, A., Piccolo, G., Perandin, F., Gorrini, C., Peruzzi, S., Zuelli, C., Ricci, L., Manca, N., Dettori, G., Chezzi, C. and Snounou, G. (2007). Genetic Polymorphisms Influence Plasmodium ovale PCR Detection Accuracy. Journal of Clinical Microbiology 1624–1627.CrossRefGoogle ScholarPubMed
Druilhe, P. and Pérignon, J-L. (1997). A hypothesis about the chronicity of malaria. Parasitology Today 13, 353–357.CrossRefGoogle ScholarPubMed
Frevert, U, Späth, G. F. and Yee, H. (2008). Exoerythrocytic development of Plasmodium gallinaceum in the White Leghorn chicken. International Journal for Parasitology 38, 655–672.CrossRefGoogle ScholarPubMed
Gardner, M. J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R. W., Carlton, J. M., Pain, A., Nelson, K. E., Bowman, S., Paulsen, I. T., James, K., Eisen, J. A., Rutherford, K., Salzberg, S. L., Craig, A., Kyes, S., Chan, M. S., Nene, V., Shallom, S. J., Suh, B., Peterson, J., Angiuoli, S., Pertea, M., Allen, J., Selengut, J., Haft, D., Mather, M. W., Vaidya, A. B., Martin, D. M., Fairlamb, A. H., Fraunholz, M. J., Roos, D. S., Ralph, S. A., McFadden, G. I., Cummings, L. M., Subramanian, G. M., Mungall, C., Venter, J. C., Carucci, D. J., Hoffman, S. L., Newbold, C., Davis, R. W., Fraser, C. M. and Barrell, B. (2002). Genome sequence of the human malaria parasite Plasmodium falciparum . Nature, London 419, 498–511.CrossRefGoogle ScholarPubMed
Handunnetti, S. M., Mendis, K. N. and David, P. H. (1987). Antigenic variation of cloned Plasmodium fragile in its natural host Macaca sinica . Sequential appearance of successive variant antigenic types. Journal of Experimental Medicine 65, 1269–83.CrossRefGoogle Scholar
Hill, A. V. S., Catherine, E. M. A., Dominic, K., Nicholas, M. A., Patrick, T., Pamela, A. R., Stephen, B., David, B., Andrew, J. M. and Brian, M. G. (1991). Common West African HLA antigens are associated with protection from severe malaria. Nature, London 352, 595–600.CrossRefGoogle ScholarPubMed
Hellgren, O., Waldenström, J., Pérez -Tris, J., Szöllosi, E., Hasselquist, D., Krizanauskiene, A., Ottosson, U. and Bensch, S. (2007). Detecting shifts of transmission areas in avian blood parasites-a phylogenetic approach. Molecular Ecology 16, 1281–1290.CrossRefGoogle Scholar
Iezhova, T. A., Valkiūnas, G. and Bairlein, F. (2005). Vertebrate host specificity of two avian malaria parasites of the subgenus Novyella: Plasmodium nucleophum and Plasmodium vaughani . Journal of Parasitology 91, 472–474.CrossRefGoogle ScholarPubMed
Kloch, A., Babik, W., Bajer, A., Sin′ski, E. and Radwan, J. (2010). Effects of an MHC-DRB genotype and allele number on the load of gut parasites in the bank vole Myodes glareolus . Molecular Ecology 19, 255–265.CrossRefGoogle ScholarPubMed
Krogstad, D. J. (1995). Plasmodium species (malaria). In Mandell, Douglas and Bennett's Principles and Practice of Infectious Diseases, 4th Edn. Vol. 2, (ed. Mandell, G. L., Bennett, J. E. and Dolin, R.), pp. 2415–2427. Churchill Livingstone, New York, USA.Google Scholar
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.CrossRefGoogle ScholarPubMed
Marinho, C. R. F., Lima, M. R. D., Grisotto, M. G. and Alvarez, J. M. (1999). Influence of acute-phase parasite load on pathology, parasitism, and activation of the immune system at the late chronic phase of chagas’ disease. Infection and Immunity 67, 308–318.CrossRefGoogle ScholarPubMed
McLean, S. A., Pearson, C. D. and Phillips, R. S. (1986). Antigenic variation in Plasmodium chabaudi: analysis of parent and variant populations by cloning. Parasite Immunology 8, 415–424.CrossRefGoogle ScholarPubMed
Palinauskas, V., Valkiūnas, G., Casimir, V. Bolshakov, C. V. and Bensch, S. (2010). Plasmodium relictum (lineage SGS1) and Plasmodium ashfordi (lineage GRW2): The effects of the co-infection on experimentally infected passerine birds . Experimental Parasitology 127, 527–533.CrossRefGoogle ScholarPubMed
Round, P. D., Hansson, B., Pearson, D. J., Kennerley, P. R. and Bensch, S. (2007). Lost and found: The enigmatic large-billed reed warbler Acrocephalus orinus rediscovered after 139 years. Journal of Avian Biology 38, 133–138.Google Scholar
Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning, a Labratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA.Google Scholar
Suounou, G., Jarra, W. and Preiser, P. R. (2000). Malaria multigene families: The price of chronicity. Parasitology today 16, 28–30.CrossRefGoogle Scholar
Valkiūnas, G. (2005). Avian malaria parasites and other haemosporidia. CRC Press, Boca Raton, FL, USA.Google Scholar
Valkiūnas, G., Zickus, T., Shapoval, A. P. and Lezhova, T. A. (2006). Effects of Haemoproteus belopolsky (Haemosporidia, Haemoproteidae) on body mass of black cap Sylvia atricapilla . Journal of Parasitology 92, 1311–1322.CrossRefGoogle Scholar
Waldenström, J., Bensch, S., Kiobi, , Hasselquist, D. and Ottoson, U. (2002). Cross species infection in blood parasite between resident and migratory songbirds in Africa. Molecular Ecology 11, 1545–1554.CrossRefGoogle ScholarPubMed
Westerdahl, H., Asghar, M., Hasselquist, D. and Bensch, S. (2011). Quantitative disease resistance: to better understand parasite-mediated selection on major histocompatibility complex. Proceedings of the Royal Societyof London, B 00, 1–8. doi:10.1098/rspb.2011.0917 Google Scholar
Westerdahl, H., Waldenström, J., Hansson, B., Hasselquist, D., von Schantz, T. and Bensch, S. (2005). Associations between malaria and MHC genes in a migratory songbird. Proceedings of the Royal Society of London, B 272, 1511–1518.Google Scholar
Woodworth, B. L., Atkinson, C. T., LaPointe, D. A., Hart, P. J., Spiegel, C. S., Tweed, E. J., Henneman, C., LeBrun, J., Denette, T., DeMots, R., Kozar, K. L., Triglia, D., Gregor, A., Smith, T. and Duffy, D. (2005). Host population persistence in the face of introduced vector-borne diseases: Hawii amakihi and avian malaria. Proceedings of the National Academy of Sciences, USA 102, 1531–1536.CrossRefGoogle Scholar
Zehtindjiev, P., Ilieva, M., Westerdahl, H., Hansson, B., Valkiūnas, G. and Bensch, S. (2008). Dynamics of parasitemia of malaria parasites in a naturally and experimentally infected migratory songbird, the great reed warbler Acrocephalus arundinaceus . Experimental Parasitology 119, 99–110.CrossRefGoogle Scholar
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