Skip to main content
×
Home

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

  • E. S. MARTINSEN (a1), J. L. WAITE (a1) and J. J. SCHALL (a1)
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.

Copyright
Corresponding author
Tel: +802 656 0702. Fax: +802 656 2914. E-mail: ellen.martinsen@uvm.edu
References
Hide All

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. 1948. 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, 683685.
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, 38293844.
Corradetti, A., Garnham, P. C. C. and Laird, M. ( 1963). New classification of the avian malaria parasites. Parassitologia 5, 14.
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, 81248129.
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, 36.
Huelsenbeck, J. P. and Ronquist, F. ( 2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755.
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, 769773.
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, 781816.
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, 435439.
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, 279288.
Perez-Tris, J., Hallelquist, D., Hellgren, O., Drizanauskiene, A., Waldenstrom, J. and Bensch, S. ( 2005). What are malaria parasites? Trends in Parasitology 21, 209211.
Perkins, S. L. and Schall, J. J. ( 2002). A molecular phylogeny of malaria parasites recovered from cytochrome b gene sequences. Journal of Parasitology 88, 972978.
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).
Posada, D. and Crandall, K. A. ( 1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.
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, 11141116.
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, 768774.
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, 357358.
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, 317327.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 6
Total number of PDF views: 13 *
Loading metrics...

Abstract views

Total abstract views: 449 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 21st November 2017. This data will be updated every 24 hours.