Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-27T12:22:46.811Z Has data issue: false hasContentIssue false

Molecular phylogenetic and morphological analysis of haemosporidian parasites (Haemosporida) in a naturally infected European songbird, the blackcap Sylvia atricapilla, with description of Haemoproteus pallidulus sp. nov.

Published online by Cambridge University Press:  21 September 2009

ASTA KRIŽANAUSKIENĖ*
Affiliation:
Institute of Ecology, Vilnius University, Akademijos 2, LT-08412 Vilnius, Lithuania
JAVIER PÉREZ-TRIS
Affiliation:
Departamento de Zoología y Antropología Física, Facultad de Biologia, Universidad Complutense de Madrid, E-28040, Madrid, Spain
VAIDAS PALINAUSKAS
Affiliation:
Institute of Ecology, Vilnius University, Akademijos 2, LT-08412 Vilnius, Lithuania
OLOF HELLGREN
Affiliation:
The EGI, Department of Zoology, South Parks Road, Oxford OX1 3PS, UK
STAFFAN BENSCH
Affiliation:
Department of Animal Ecology, Lund University, Ecology Building, SE-223 62 Lund, Sweden
GEDIMINAS VALKIŪNAS
Affiliation:
Institute of Ecology, Vilnius University, Akademijos 2, LT-08412 Vilnius, Lithuania
*
*Corresponding author: Institute of Ecology, Vilnius University, Akademijos 2, LT-08412 Vilnius, Lithuania. Tel: + 370 5 272 92 69. Fax: + 370 5 272 93 52. E-mail: asta@ekoi.lt

Summary

The blackcap (Sylvia atricapilla) is a common Palearctic migratory warbler, and haemosporidian parasites are common in this species. However, genetic and phenotypic diversity of haemosporidians in warblers has been insufficiently investigated and poorly linked. We addressed this issue by combining molecular and microscopy data for detection of pigment-forming haemosporidians of the genera Haemoproteus and Plasmodium. Blood samples from 498 blackcaps were collected at 7 different sites in Europe and investigated for these parasites by polymerase chain reaction (PCR)-based techniques and microscopic examination. In all, 56% of the birds were infected by at least 1 out of 25 distinct mitochondrial cytochrome b (cyt b) gene lineages of these haemosporidians. It is concluded that the blackcap is infected not only with blackcap specific haemosporidians, but also with Haemoproteus majoris, which is a host generalist and common in birds belonging to the Paridae. Haemoproteus pallidulus sp. nov. is described based on morphology of its blood stages and segments of the cyt b and dihydrofolate reductase/thymidylate synthase (DHFR-TS) genes. This study provides evidence that genetic diversity of haemosporidian parasites might be positively correlated with migratory strategies of their avian hosts; it also contributes to the value of both microscopy and molecular diagnostics of avian blood parasites.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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

Atkinson, C. T. and van Riper, C. III (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, UK.CrossRefGoogle Scholar
Bennett, G. F. and Campbell, A. G. (1972 a). Avian Haemoproteidae. I. Description of Haemoproteus fallisi n. sp. and a review of the haemoproteids of the family Turdidae. Canadian Journal of Zoology 50, 12691275.CrossRefGoogle Scholar
Bennett, G. F., Okia, N. O., Ashford, R. W. and Campbell, A. G. (1972 b). Avian Haemoproteidae. II. Haemoproteus enucleator sp. n. from the Kingfisher, Ispidina picta (Boddaert). Journal of Parasitology 58, 11431147.Google Scholar
Bennett, G. F. and Peirce, M. (1991). The haemoproteids of the weaver finches (Passeriformes). Journal of Natural History 25, 7–22.CrossRefGoogle Scholar
Bensch, S., Hellgren, O. and Pérez-Tris, J. (2009). MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources 9, 13531358.CrossRefGoogle ScholarPubMed
Bensch, S., Pérez-Tris, J., Waldenström, J. and Hellgren, O. (2004). Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: Multiple cases of cryptic speciation? Evolution 58, 16171621.Google Scholar
Bensch, S., Stjenman, M., Hasselquist, D., Östman, Ö., Hansson, B., Westerdahl, H. and Torres-Pinheiro, R. (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 276, 15831589.Google Scholar
Cramp, S. (1992). The Birds of the Western Palearctic. Vol. VI. Oxford University Press, Oxford, UK.Google Scholar
Fallon, S., Bermingham, E. and Ricklefs, E. (2003). Island and taxon effects in parasitism revisited: avian malaria in the Lesser Antilles. Evolution 57, 606615.Google ScholarPubMed
Feldman, R. A., Freed, L. A. and Cann, R. L. (1995). A PCR test for avian malaria in Hawaiian birds. Molecular Ecology 4, 663673.Google Scholar
Garnham, P. C. C. (1966). Malaria Parasites and other Haemosporidia. Blackwell Scientific Publications, Oxford, UK.Google Scholar
Godfrey, R. D., Fedynich, A. M. and Pence, D. B. (1987). Quantification of hematozoa in blood smears. Journal of Wildlife Diseases 23, 558565.Google Scholar
Hall, T. A. (1999). BioEdit: A user – friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symposium 41, 9598.Google Scholar
Hellgren, O., Waldenström, J. and Bensch, S. (2004). A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. Journal of Parasitology 90, 797802.CrossRefGoogle ScholarPubMed
Hellgren, O., Križanauskienė, A., Valkiūnas, G. and Bensch, S. (2007 a). Diversity and phylogeny of mitochondrial cytochrome b lineages from six morphospecies of avian Haemoproteus (Haemosporida, Haemoproteidae). Journal of Parasitology 93, 889896.CrossRefGoogle ScholarPubMed
Hellgren, O., Waldenström, J., Pérez-Tris, J., Szöllősi, E., Hasselquist, D., Križanauskienė, A., Ottosson, U. and Bensch, S. (2007 b). Detecting shifts of transmission areas in avian blood parasites – a phylogenetic approach. Molecular Ecology 16, 12811290.CrossRefGoogle ScholarPubMed
Križanauskienė, A., Hellgren, O., Kosarev, V., Sokolov, L., Bensch, S. and Valkiūnas, G. (2006). Variation in host specificity between species of avian haemosporidian parasites: evidence from parasite morphology and cytochrome b gene sequences. Journal of Parasitology 92, 13191324.Google Scholar
Kumar, S., Tamura, K. and Nei, M. (2004). MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5, 150163.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Martinsen, E. S, Perkins, S. 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
Nylander, J. A. A. (2004). MrModeltest v2. Program distributed by the author. Software avialable at: http://www.ebc.uu.se/systzoo/staff/nylander.html. Evolutionary Biology Centre, Uppsala University, Finland.Google Scholar
Palinauskas, V., Kosarev, V., Shapoval, A., Bensch, S. and Valkiūnas, G. (2007). Comparison of mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites of the subgenera Haemamoeba and Giovannolaia (Haemosporida: Plasmodiidae). Zootaxa 1626, 3950.Google Scholar
Pérez-Tris, J. and Bensch, S. (2005 a). Dispersal increases local transmission of avian malarial parasites. Ecology Letters 8, 838845.CrossRefGoogle Scholar
Pérez-Tris, J. and Bensch, S. (2005 b). Diagnosing genetically diverse avian malaria infections using mixed-sequence analysis and TA-cloning. Parasitology 131, 19.CrossRefGoogle ScholarPubMed
Pérez-Tris, J., Bensch, S., Carbonell, R., Helbig, A. J. and Telleria, J. L. (2004). Historical diversification of migration patterns in a passerine bird. Evolution 58, 18191832.CrossRefGoogle Scholar
Perez-Tris, J, Hellgren, O., Križanauskienė, A., Waldenstrom, J., Secondi, J., Bonneaud, C., Fjeldsa, J., Hasselquist, D. and Bensch, S. (2007). Within-host speciation of malaria parasites. PloS One 2, e235.Google Scholar
Perkins, S. L. and Schall, J. J. (2002). A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. Journal of Parasitology 88, 972978.CrossRefGoogle ScholarPubMed
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.CrossRefGoogle ScholarPubMed
Valkiūnas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, FL, USA.Google Scholar
Valkiūnas, G., Bensch, S., Iezhova, T. A., Križanauskienė, A., Hellgren, O. and Bolshakov, C. (2006). Nested cytochrome b polymerase chain reaction diagnostics underestimate mixed infections of avian blood haemosporidian parasites: microscopy is still essential. Journal of Parasitology 92, 418422.CrossRefGoogle ScholarPubMed
Valkiūnas, G. and Iezhova, T. A. (1991). New species of haemoproteids (Haemosporidia) in passerine birds. Parazitologiya (St. Petersburg) 25, 212218 (in Russian).Google Scholar
Valkiūnas, G. and Iezhova, T. A. (1992). New species of haemoproteids (Haemosporidia: Haemoproteidae) in passerine birds. Zoolgicheskij zhurnal (Moscow) 71, 5–15 (in Russian).Google Scholar
Valkiūnas, G., Iezhova, T. A., Križanauskienė, A., Palinauskas, V., Bensch, S. (2008 c). In vitro hybridization of Haemoproteus spp.: an experimental approach for direct investigation of reproductive isolation of parasites. Journal of Parasitology 94, 13851394.CrossRefGoogle ScholarPubMed
Valkiūnas, G., Iezhova, T. A., Križanauskienė, A., Palinauskas, V. and Bensch, S. (2008 d). A comparative analysis of microscopy and PCR-based detection methods for blood parasites. Journal of Parasitology 94, 13951401.CrossRefGoogle ScholarPubMed
Valkiūnas, G., Iezhova, T. A., Loiseau, C., Chasar, A., Thomas, B. S. and Sehgal, R. N. M. (2008 a). New species of haemosporidian parasites (Haemosporida) from African rainforest birds, with remarks on their classification. Parasitology Research 103, 12131228.CrossRefGoogle ScholarPubMed
Valkiūnas, G., Križanauskienė, A., Iezhova, T. A., Hellgren, O. and Bensch, S. (2007). Molecular phylogenetic analysis of circumnuclear hemoproteids (Haemosporida: Haemoproteidae) of sylviid birds, with a description of Haemoproteus parabelopolskyi sp. nov. Journal of Parasitology 93, 680687.Google Scholar
Valkiūnas, G., Zehtindjiev, P., Dimitrov, D., Križanauskienė, A., Iezhova, T. A. and Bensch, S. (2008 b). Polymerase chain reaction-based identification of Plasmodium (Huffia) elongatum, with remarks on species identity of haemosporidian lineages deposited in GenBank. Parasitology Research 102, 11851193.CrossRefGoogle ScholarPubMed
Waldenström, J., Bensch, S., Hasselquist, D. and Östman, Ö. (2004). A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology 90, 191194.CrossRefGoogle ScholarPubMed
Žalakevičius, M. (1986). Migration of Birds. Mokslas Press, Vilnius, Lithuania (in Lithuanian).Google Scholar