Hostname: page-component-89b8bd64d-shngb Total loading time: 0 Render date: 2026-05-07T11:14:11.939Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphological versus molecular identification of avian Haemosporidia: an exploration of three species concepts

Published online by Cambridge University Press:  02 June 2006

E. S. MARTINSEN ,
I. PAPERNA  and
J. J. SCHALL
E. S. MARTINSEN
Affiliation:
Department of Biology, University of Vermont, Burlington, Vermont 05405, USA
I. PAPERNA
Affiliation:
Department of Animal Sciences, Faculty of Agriculture, Food and Environmental Quality, The Hebrew University of Jerusalem, Rehovot, Israel
J. J. SCHALL
Affiliation:
Department of Biology, University of Vermont, Burlington, Vermont 05405, USA
Get access Rights & Permissions [Opens in a new window]

Abstract

More than 200 species of avian Haemosporidia (genera Plasmodium, Haemoproteus, and Leucocytozoon) have been described based primarily on morphological characters seen in blood smears. Recent molecular studies, however, suggest that such methods may mask a substantial cryptic diversity of avian haemosporidians. We surveyed the haemosporidians of birds sampled at 1 site in Israel. Parasites were identified to species based on morphology, and a segment of the parasite's cytochrome b gene was sequenced. We compared 3 species concepts: morphological, genetic, and phylogenetic. Fifteen morphological species were present. Morphological species that occurred once within our dataset were associated with a unique gene sequence, displayed large genetic divergence from other morphological species, and were not contained within clades of morphological species that occurred more than once. With only 1 exception, morphological species that were identified from multiple bird hosts presented identical sequences for all infections, or differed by few synonymous substitutions, and were monophyletic for all phylogenetic analyses. Only the morphological species Haemoproteus belopolskyi did not follow this trend, falling instead into at least 2 genetically distant clades. Thus, except for H. belopolskyi, parasites identified to species by morphology were supported by both the genetic and phylogenetic species concepts.

Keywords

haemosporidiaPlasmodiumHaemoproteusLeucocytozoonavian malaria parasitesspecies conceptscytochrome b

Information

Type
Research Article
Information
Parasitology , Volume 133 , Issue 3 , September 2006 , pp. 279 - 288
Copyright
2006 Cambridge University Press

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.)

Article purchase

Temporarily unavailable

References

REFERENCES

Atkinson, C. T., Woods, K. L., Dusek, R. J., Sileo, L. S. and Iko, W. M. ( 1995). Wildlife disease and conservation in Hawaii: Pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected Iiwi (Vestiaria coccinea). Parasitology 111, 59–69.CrossRefGoogle Scholar
Beadell, J. S., Gering, E., Austin, J., Dumbacher, J. P., Pierce, 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
Bennett, G. F. and Campbell, A. G. ( 1972). Avian Haemoproteidae 1. Description of Haemoproteus fallisi n.sp. and a review of the haemoproteids of the family Turdidae. Canadian Journal of Zoology 50, 1269–1275.Google Scholar
Bennett, G. F., Earlé, R. A. and Peirce, M. A. ( 1992). The Leucocytozoidae of South African birds: Passeriformes. Onderstepoort Journal of Veterinary Research 59, 235–247.Google Scholar
Bennett, G. F., Kucera, J., Woodworth-Lynas, C. and Whiteway, M. ( 1981). Bibliography of the avian blood-inhabiting Protozoa. Supplement 1. Memorial University of Newfoundland Occasional Papers in Biology 4, 1–33.Google Scholar
Bensch, S. and Akesson, S. ( 2003). Temporal and spatial variation of haematozoans in Scandanavian willow warblers. Journal of Parasitology 89, 388–391.CrossRefGoogle Scholar
Bensch, S., Stjernman, M., Hasselquist, D., Ostman, O., Hansson, B., Westerdahl, H. and Pinheiro, R. T. ( 2000). Host specificity in 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 Scholar
Bensch, S., Perex-Tris, J., Waldenstrom, J. and Hellgren, O. ( 2004). Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution 58, 1617–1621.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. Evolution 95, 8124–8129.CrossRefGoogle Scholar
Fallon, S. M., Ricklefs, R. E., Latta, S. C. and Bermingham, E. ( 2003 a). Temporal stability of insular avian malarial parasite communities. Proceedings of the Royal Society of London, B 271, 493–500.Google Scholar
Fallon, S. M., Ricklefs, R. E., Swanson, B. L. and Bermingham, E. ( 2003 b). Detecting avian malaria: an improved polymerase chain reaction diagnostic. Journal of Parasitology 89, 1044–1047.Google Scholar
Fallon, S. M., Bermingham, E. and Ricklefs, R. E. ( 2005). Host specialization and geographic localization of avian malaria parasites: A regional analysis in the Lesser Antilles. The American Naturalist 165, 466–480.CrossRefGoogle Scholar
Garnham, P. C. C. ( 1966). Malaria Parasites and other Haemosporidia. Blackwell Scientific Publications, Oxford.
Heinzel, H., Fitter, R. and Paralow, J. ( 1972). The Birds of Britain and Europe with North Africa and the Middle East. Collins, London.
Hellgren, O. ( 2005). The occurrence of haemosporidian parasites in the Fennoscandian bluethroat (Luscinia svecica) population. Journal of Ornithology 146, 55–60.CrossRefGoogle Scholar
Huelsenbeck, J. P. and Ronquist, F. ( 2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.CrossRefGoogle Scholar
Joy, D. A., Feng, X., Mu, J., Furuya, T., Chotivanich, K., Krettli, A. U., Ho, M., Wang, A., White, N. J., Suh, E., Beerli, P. and Su, X.-Z. ( 2003). Early origin and recent expansion of Plasmodium falciparum. Science 300, 318–321.CrossRefGoogle Scholar
Khan, R. A. and Fallis, A. M. ( 1970). Life cycles of Leucocytozoon dubreuili Mathis and Leger, 1911 and L. fringillinarum Woodcock, 1910 (Haemosporidia: Leucocytozoidae). Journal of Protozoology 17, 642–658.Google Scholar
Kissinger, J. C., Souza, P. C. Al., 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
Laird, M. ( 1998). Avian Malaria in the Asian Tropical Subregion. Springer, Singapore.
Landau, I., Chabaud, A. G., Bretani, S. and Snounou, G. ( 2003). Taxonomic status and redescription of Plasmodium relictum (Grassi et Felletti, 1891), Plasmodium maior Raffaele, 1931, and description of P. bigueti in sparrows. Parassitologia 45, 119–123.Google Scholar
Levine, N. D. ( 1988). The Protozoa Plylum Apicomplexa, Vol. II. CRC Press, Boca Raton, Florida, USA.
Maddison, D. R. and Maddison, W. P. ( 2001). MacClade 4: Analysis of Phylogeny and Character Evolution. Version 4.02. Sinauer Associates, Sunderland, Massachusetts, USA.
Mayden, R. L. ( 1997). A hierarchy of species concepts: the denouement in the saga of the species problem. In Species, the Units of Biodiversity ( ed. Claridge, M. F., Dawah, H. A. and Wilson, M. R.), pp. 381–424. Chapman and Hall, London.
Noland, G. S., Briones, N. and Sullivan, D. J. ( 2003). The shape and size of hemozoin crystals distinguishes diverse Plasmodium species. Molecular and Biochemical Parasitology 130, 91–99.CrossRefGoogle Scholar
Perkins, S. L. ( 2000). Species concepts and malaria parasites: detecting a cryptic species of Plasmodium. Proceedings of the Royal Society of London, B 267, 2345–2350.CrossRefGoogle Scholar
Perkins, S. L. and Schall, J. J. ( 2002). A molecular phylogeny of malaria parasites recovered from cytochrome b gene sequences. Journal of Parasitology 8, 972–978.CrossRefGoogle Scholar
Posada, D. and Crandall, K. A. ( 1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle Scholar
Poulin, R. and Morand, S. ( 2004). Parasite Biodiversity. Smithsonian Institution Books, Washington, D.C., USA.
Ricklefs, R. E. and Fallon, S. M. ( 2002). Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society of London, B 269, 885–892.CrossRefGoogle Scholar
Ricklefs, R. E., Swanson, B. L., Fallon, S. M., Martinez-Abrain, A., Scheuerlein, A., Gray, J. and Latta, S. C. ( 2005). Community relationships of avian malaria parasites in Southern Missouri. Ecological Monographs 75, 543–559.CrossRefGoogle Scholar
Schrenzel, M. D., Maalouf, G. A., Keener, L. L. and Gaffney, P. M. ( 2003). Molecular characterization of malarial parasites in captive passerine birds. Journal of Parasitology 89, 1025–1033.CrossRefGoogle Scholar
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
Svensson, L., Mullarney, K. and Zetterström, D. ( 1999). Fägelguiden. Europe och Medelhavsområdets fåglar i fält. Albert Bonniers Förlag, Stockholm (Hebrew translation 2003, MAP – Mapping and Publishing and Hakibutz Hameuchad, Israel).
Swofford, D. L. ( 2002). PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods) 4.0 Beta. Sinauer, Sunderland, MA, USA.
Valkiunas, G. ( 2005). Avian Malaria Parasites and Other Haemosporidia. CRC Press, Boca Raton, Florida, USA.
Waldenstrom, J., Bensch, S., Kibol, S., Hasselquist, D. and Ottosson, U. ( 2002). Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Ecology 11, 1545–1554.CrossRefGoogle Scholar