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Morphologically defined subgenera of Plasmodium from avian hosts: test of monophyly by phylogenetic analysis of two mitochondrial genes

Published online by Cambridge University Press:  06 December 2006

E. S. MARTINSEN ,
J. L. WAITE  and
J. J. SCHALL
E. S. MARTINSEN
Affiliation:
Department of Biology, University of Vermont, Burlington, Vermont 05405, USA
J. L. WAITE
Affiliation:
Department of Biology, University of Vermont, Burlington, Vermont 05405, USA
J. J. SCHALL
Affiliation:
Department of Biology, University of Vermont, Burlington, Vermont 05405, USA
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Abstract

Malaria parasites in the genus Plasmodium are now placed within 11 subgenera based on morphology under the light microscope, life-history traits, and host taxon. The phylogenetic significance of these characters, however, is problematic because the observed variation could be homoplasious. Using Plasmodium infections found in 2632 birds of many avian families collected in the USA, and several samples from other locations, we compared identifications to subgenus based on morphology in blood smears with a 2-gene molecular phylogeny (the first for avian Plasmodium) to determine if the 5 avian Plasmodium subgenera represent monophyletic groups. Phylogenetic trees recovered by parsimony, likelihood, and Bayesian methods presented nearly identical topologies. The analysis allowed testing the hypothesis of monophyly for the subgenera. Monophyly of the subgenera Haemamoeba, Huffia, and Bennettinia was supported by the analysis. The distinctive morphology of Haemamoeba species appears to have evolved once. Most samples identified to Novyella also fell within a monophyletic clade with the exception of 2 samples that fell basal to all other avian Plasmodium. Samples of the subgenus Giovannolaia did not form a monophyletic group. Thus, the characters used by parasitologists for over a century to define subgenera of Plasmodium vary in their phylogenetic significance.

Keywords

Plasmodiumavian malaria parasitescytochrome bcytochrome oxidase Isubgeneramonophyly
Type
Research Article
Information
Parasitology , Volume 134 , Issue 4 , April 2007 , pp. 483 - 490
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Atkinson, C. T. and van Riper, C. ( 1991). Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In Bird-Parasite Interactions: Ecology, Evolution, and Behaviour (ed. Loye, J. E. and Zuk, M.), pp. 19–48. Oxford University Press, Oxford.
Beadell, J. S. and Fleischer, R. C. ( 2005). A restriction enzyme-based assay to distinguish between avian hemosporidians. Journal of Parasitology 91, 683–685.CrossRefGoogle Scholar
Beadell, J. S., Gering, E., Austin, J., Dumbacher, J. P., Peirce, M. A., Pratt, T. K., Atkinson, C. T. and Fleischer, R. C. ( 2004). Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Molecular Ecology 13, 3829–3844.CrossRefGoogle Scholar
Corradetti, A., Garnham, P. C. C. and Laird, M. ( 1963). New classification of the avian malaria parasites. Parassitologia 5, 1–4.Google Scholar
Escalante, A. A., Freeland, D. E., Collins, W. E. and Lal, A. A. ( 1998). The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proceedings of the National Academy of Sciences, USA 95, 8124–8129.CrossRefGoogle Scholar
Garnham, P. C. C. ( 1966). Malaria Parasites and other Haemosporidia. Blackwell Scientific Publications, Oxford.
Grassi, B. and Feletti, R. ( 1890). Parassiti malarici negli uccelli-Nota preliminaire. Bollettino. Sedute della Accademia Gioenia di Scienza Naturali in Catania 13, 3–6.Google Scholar
Huelsenbeck, J. P. and Ronquist, F. ( 2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.CrossRefGoogle Scholar
Kissinger, J. C., Souza, P. C. A., Soares, C. O., Paul, R., Wahl, A. M., Rathore, D., McCutchan, T. F. and Krettli, A. U. ( 2002). Molecular phylogenetic analysis of the avian malarial parasite Plasmodium (Novyella) juxtanucleare. Journal of Parasitology 88, 769–773.CrossRefGoogle Scholar
Kjer, K. M., Blahnik, R. J. and Holzenthal, R. W. ( 2001). Phylogeny of Trichoptera (Caddisflies): characterization of signal and noise within multiple datasets. Systematic Biology 50, 781–816.CrossRefGoogle Scholar
Laird, M. ( 1998). Avian Malaria in the Asian Tropical Subregion. Springer, Singapore.
Maddison, D. R. and Maddison, W. P. ( 2001). MacClade 4: Analysis of Phylogeny and Character Evolution. Version 4.02. Sinauer Associates, Sunderland, Massachusetts.
Manwell, R. D. ( 1936). The problem of species, with special reference to the malaria parasites. Annuals of Tropical Medicine and Hygiene 30, 435–439.CrossRefGoogle Scholar
Martinsen, E. S., Paperna, I. and Schall, J. J. ( 2006). Morphological versus molecular identification of avian Haemosporidia: an exploration of three species concepts. Parasitology 133, 279–288.CrossRefGoogle Scholar
Perez-Tris, J., Hallelquist, D., Hellgren, O., Drizanauskiene, A., Waldenstrom, J. and Bensch, S. ( 2005). What are malaria parasites? Trends in Parasitology 21, 209–211.Google Scholar
Perkins, S. L. and Schall, J. J. ( 2002). A molecular phylogeny of malaria parasites recovered from cytochrome b gene sequences. Journal of Parasitology 88, 972–978.CrossRefGoogle Scholar
Perkins, S. L., Sarkar I. N. and Carter, R. ( 2006). Phylogeny of rodent malaria parasites: simultaneous analysis across three genomes. Infection, Genetics, and Evolution (in the Press).Google Scholar
Posada, D. and Crandall, K. A. ( 1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle Scholar
Seed, T. M. and Manwell, R. D. ( 1977). Plasmodia of birds. In Parasitic Protozoa, Vol. III; Gregarines, Haemogregarines, Coccidia, Plasmodia, and Haemoproteids. Academic Press, New York.
Shimodaira, H. and Hasegawa, M. ( 1999). Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16, 1114–1116.CrossRefGoogle Scholar
Swofford, D. L. ( 2002). PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods) 4.0 Beta. Sinauer, Sunderland, MA.
Szymanski, M. M. and Lovette, I. J. ( 2005). High lineage diversity and host sharing of malarial parasites in a local avian assemblage. Journal of Parasitology 91, 768–774.CrossRefGoogle Scholar
Valkiunas, G. ( 1997). Bird Haemosporidia. Institute of Ecology, Vilnius.
Valkiunas, G. ( 2005). Avian Malaria Parasites and Other Haemosporidia. CRC Press, Boca Raton, Florida.
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.Google Scholar
van Riper, C., van Riper, S. G., Goff, M. L. and Laird, M. ( 1986). The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs 56, 317–327.Google Scholar