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Low prevalence of Haemoproteus infections in Chiffchaffs

Published online by Cambridge University Press:  11 November 2011

STAFFAN BENSCH ,
JANE JÖNSSON  and
JOSÉ LUIS COPETE
STAFFAN BENSCH*
Affiliation:
Molecular Ecology and Evolution Lab, Department of Biology, Lund University, Sweden
JANE JÖNSSON
Affiliation:
Molecular Ecology and Evolution Lab, Department of Biology, Lund University, Sweden
JOSÉ LUIS COPETE
Affiliation:
Martínez de la Rosa 27 Pral 3a, 08012 Barcelona, Spain
*
*Corresponding author: Department of biology, Ecology Building, Lund University, 223 62 Lund, Sweden. Tel: +46 46 2224292. Fax: +46 46 2224716. E-mail: staffan.bensch@biol.lu.se
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Summary

Parasite prevalence is an important variable in many evolutionary and ecological studies. In birds, haemosporidian blood parasites have been in focus of many comparative analyses. Because low prevalence is difficult to estimate precisely and that studies finding low prevalence are more likely to remain unpublished, our knowledge of parasite prevalence is biased towards highly infected taxa. Species with naturally low levels of infection are nonetheless interesting as they may provide models for studying the evolution of pathogen resistance. In the present study we show that the prevalence of Haemoproteus parasites is markedly lower in several taxa within the widely distributed chiffchaff species-complex compared to other species within the genus Phylloscopus. Since chiffchaffs, P. collybita, commonly coexists in the same habitat as congeners frequently infected with Haemoproteus parasites, immediate ecological variables like abundance of vectors can hardly explain this difference. Some of the parasites infecting coexisting congeners are broad host generalists leaving it enigmatic why chiffchaffs are almost free of Haemoproteus infections. We propose that detailed infection experiments are needed to illuminate whether chiffchaffs possess a genetic immunity against Haemoproteus parasites or if other more subtle ecological processes, like anti-vector behaviour, play a role in its generally low level of infestation.

Keywords

Phylloscopus collybitaHaemoproteusPlasmodiumLeucocytozoonprevalence
Type
Research Article
Information
Parasitology , Volume 139 , Issue 3 , March 2012 , pp. 302 - 309
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Allander, K. and Bennett, G. F. (1994). Prevalence and intensity of haematozoan infection in a population of great tits Parus major from Gotland, Sweden. Journal of Avian Biology 25, 69–74.CrossRefGoogle Scholar
Apanius, V., Yorinks, N., Bermingham, E. and Ricklefs, R. E. (2000). Island and taxon effects in parasitism and resistance of Lesser Antillean birds. Ecology 81, 1959–1969.CrossRefGoogle Scholar
Beadell, J. S., Ishtiaq, F., Covas, R., Melo, M., Warren, B. H., Atkinson, C. T., Bensch, S., Graves, G. R., Jhala, Y. V., Peirce, M. A., Rahmani, A. R., Fonseca, D. M. and Fleischer, R. C. (2006). Global phylogeographic limits of Hawaii's avian malaria. Proceedings of the Royal Society of London, B 273, 2935–2944.Google ScholarPubMed
Bensch, S. and Åkesson, S. (2003). Temporal and spatial variation of Hematozoans in Scandinavian willow warblers. Journal of Parasitology 89, 388–391.CrossRefGoogle ScholarPubMed
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, 1353–1358.CrossRefGoogle ScholarPubMed
Bensch, S., Stjernman, 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 267, 1583–1589.CrossRefGoogle ScholarPubMed
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. American Naturalist 165, 466–480.CrossRefGoogle ScholarPubMed
Freed, L. A. and Cann, R. L. (2006). DNA quality and accuracy of avian malaria PCR diagnostics: a review. Condor 108, 459–473.CrossRefGoogle Scholar
Freeman-Gallant, C. R., O'Connor, K. D. and Breuer, M. E. (2001). Sexual selection and geography of Plasmodium infection in savannah sparrows (Passerculus sandwichensis). Oecologia 127, 517–521.CrossRefGoogle ScholarPubMed
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hamilton, W. D. and Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387.CrossRefGoogle Scholar
Hansson, M., Bensch, S. and Brännström, O. (2000). Range expansion and the possibility of an emerging contact zone between two subspecies of Chiffchaff Phylloscopus collybita ssp. Journal of Avian Biology 31, 548–558.CrossRefGoogle Scholar
Helbig, A. J., Martens, J., Seibold, I., Henning, F., Schottler, B. and Wink, M. (1996). Phylogeny and species limits in the Palaearctic chiffchaff Phylloscopus collybita complex: mitochondrial genetic differentiation and bioacoustic evidence. Ibis 138, 650–666.CrossRefGoogle Scholar
Helbig, A. J., Salomon, M., Bensch, S. and Seibold, I. (2001). Male-biased gene flow across an avian hybrid zone: evidence from mitochondrial and microsatellite DNA. Journal of Evolutionary Biology 14, 277–287.CrossRefGoogle Scholar
Hellgren, O., Pérez-Tris, J. and Bensch, S. (2009). A jack-of-all-trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology 90, 2840–2849.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, 797–802.Google ScholarPubMed
Hellgren, O., Waldenström, J., Pérez-Tris, J., Szöllōsi, 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 ScholarPubMed
Ishtiaq, F., Gering, E., Rappole, J. H., Rahmani, A. R., Jhala, Y. V., Dove, C. J., Melinsky, C., Olson, S. L., Peirce, M. A. and Fleischer, R. C. (2007). Prevalence and diversity of avian hematozoan parasites in asia: a regional survey. Journal of Wildlife Diseases 43, 382–398.CrossRefGoogle Scholar
Jovani, R. and Tella, J. L. (2006). Parasite prevalence and sample size: misconceptions and solutions. Trends in Parasitology 22, 214–218.CrossRefGoogle ScholarPubMed
Krizanauskiene, A., Pérez-Tris, J., Palinauskas, V., Hellgren, O., Bensch, S. and Valkiūnas, G. (2010). Molecular phylogenetic and morphological analysis of haemosporiian parasites (Haemosporida) in a naturally infected European songbird, the blackcap Sylvia atricapilla, with description of Haemoproteus pallidulus sp. nov. Parasitology 137, 217–227.CrossRefGoogle Scholar
Lee, K. A., Martin II, L. B., Hasselquist, D., Ricklefs, R. E. and Wikelski, M. (2006). Contrasting adaptive immune defenses and blood parasite prevalence in closely related Passer sparrows. Oecologia 150, 383–392.CrossRefGoogle ScholarPubMed
MacLeod, C. J., Paterson, A. M., Tompkins, D. M. and Duncan, R. P. (2010). Parasites lost – do invaders miss the boat or drown on arrival? Ecology Letters 13, 516–527.CrossRefGoogle ScholarPubMed
Malmqvist, B., Strasevicius, D., Hellgren, O., Adler, P. S. and Bensch, S. (2004). Vertebrate host specificity of wild-caught blackflies revealed by mtDNA in blood. Proceedings of the Royal Society of London, B (Suppl.) 271, S152–S155.CrossRefGoogle ScholarPubMed
Mendes, L., Piersma, T., Lecoq, M., Spaans, B. and Ricklefs, R. E. (2005). Disease-limited distributions? Contrasts in the prevalence of avian malaria in shorebird species using marine and freshwater habitats. Oikos 109, 396–404.CrossRefGoogle Scholar
Møller, A. P. (2008). Flight distance and blood parasites in birds. Behavioral Ecology 19, 1305–1313.Google Scholar
Nacher, M. (2004). Interactions between worm infections and malaria. Clinical Reviews in Allergy and Immunology 26, 85–92.Google ScholarPubMed
Palinauskas, V., Valkiūnas, G., Bolshakov, C. V. and Bensch, S. (2008). Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds. Experimental Parasitology 120, 372–380.CrossRefGoogle ScholarPubMed
Peirce, M. A. (1981). Distribution and host-parasite check-list of haematozoa of birds in Western Europe. Journal of Natural History 15, 419–458.CrossRefGoogle Scholar
Peirce, M. A. and Mead, C. J. (1984). Haematozoa of British birds VIII. Blood parasites of migrants, particularly the willow warbler Phylloscopus trochilus. Journal of Natural History 18, 335–340.CrossRefGoogle Scholar
Pérez-Tris, J. and Bensch, S. (2005 a). Diagnosing genetically diverse avian malaria infections using mixed-sequence analysis and TA-cloning. Parasitology 131, 15–23.CrossRefGoogle ScholarPubMed
Pérez-Tris, J. and Bensch, S. (2005 b). Dispersal increases local transmission of avian malarial parasites. Ecology Letters 8, 838–845.CrossRefGoogle Scholar
Pérez-Tris, J., Hellgren, O., Krizanauskiene, A., Waldenström, J., Secondi, J., Bonneaud, C., Fjeldså, J., Hasselquist, D. and Bensch, S. (2007). Within-host speciation of malaria parasites. PloS ONE 2, e235. doi:10.1371/journal.pone.0000235.CrossRefGoogle ScholarPubMed
Piersma, T. (1997). Do global patterns of habitat use and migration strategies co-evolve with relative investments in immunocompetence due to spatial variation in parasite pressure? Oikos 80, 623–631.CrossRefGoogle Scholar
Reullier, J., Pérez-Tris, J., Bensch, S. and Secondi, J. (2006). Diversity, distribution and exchange of blood parasites meeting at an avian moving contact zone. Molecular Ecology 15, 753–763.Google ScholarPubMed
Richie, T. L. (1988). Interactions between malaria parasites infecting the same vertebrate host. Parasitology 96, 607–639.CrossRefGoogle ScholarPubMed
Richman, A. (1996). Ecological diversification and community structure in the old world leaf warblers (Genus Phylloscopus): a phylogenetic perspective. Evolution 50, 2461–2470.Google ScholarPubMed
Ricklefs, R. E. (1992). Embryonic development period and the prevalence of avian malaria parasites. Proceedings of the National Academy of Sciences, USA 89, 4722–4725.CrossRefGoogle Scholar
Ricklefs, R. E. (2010). Host-pathogen coevolution, secondary sympatry and species diversification. Philosophical Transaction of the Royal Society of London, B 365, 1139–1147.Google ScholarPubMed
Rintamäki, P. T., Ojanen, W., Pakkala, H. and Tynjala, M. (1998). Blood parasites of migrating Willow Warblers (Phylloscopus trochilus) at a stopover site. Canadian Journal of Zoology 76, 984–988.CrossRefGoogle Scholar
Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular cloning, a laboratory manual, 2 edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA.Google Scholar
Santiago-Alarcon, D., Bloch, R., Rolshausen, G., Schaefer, H. M. and Segelbacher, G. (2011). Prevalence, diversity, and interaction patterns of avian haemosporidians in a four-year study of blackcaps in a migratory divide. Parasitology 138, 824–835.CrossRefGoogle Scholar
Scheuerlein, A. and Ricklefs, R. E. (2004). Prevalence of blood parasites in European passerine birds. Proceedings of the Royal Society of London, B 271, 1363–1370.CrossRefGoogle Scholar
Stjernman, M., Råberg, L. and Nilsson, J.-Å. (2008). Maximum host survival at intermediate parasite infection intensities. PloS ONE 3, e2463. doi:10.1371/journal.pone.0002463.CrossRefGoogle ScholarPubMed
Svensson, S., Svensson, M. and Tjernberg, M. (1999). Svensk fågelatlas. Vår Fågelvärld Suppl. 31.Google Scholar
Tella, J. L., Blanco, G., Forero, M. G., Gajón, Á., Donázar, J. A. and Hiraldo, F. (1999). Habitat, world geographic range and development of hosts explain the prevalence of avian hematozoa at small spatial and phylogenetic range. Proceedings of the National Academy of Sciences, USA 96, 1785–1789.CrossRefGoogle Scholar
Tompkins, D. M., White, A. and Boots, M. (2003). Ecological replacement of native red squirrels by invasive greys driven by disease. Ecology Letters 6, 189–196.CrossRefGoogle Scholar
Valkiūnas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, FL, USA.Google Scholar
Valkiūnas, G. and Iezhova, T. A. (2004). The transmission of Haemoproteus belopolskyi (Haemosporida: Haemoproteidae) of blackcap by Culicoides impunctatus (Diptera: Ceratopogonidae). Journal of Parasitology 90, 196–198.CrossRefGoogle ScholarPubMed
Valkiūnas, G., Iezhova, T. A., Krizanauskiene, A., Palinauskas, V., Sehgal, R. N. M. and Bensch, S. (2008). A comparative analysis of microscopy and PCR-based detection methods for blood parasites. Journal of Parasitology 94, 1395–1401.CrossRefGoogle ScholarPubMed
Waldenström, J., Bensch, S., Hasselquist, D. and Östman, Ö. (2004). A new nested PCR method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology 90, 191–194.CrossRefGoogle ScholarPubMed
Waldenström, J., Bensch, S., Kiboi, 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 ScholarPubMed
Wood, M. J., Cosgrove, C. L., Wilkin, T. A., Knowles, S. C. L., Day, K. P. and Sheldon, B. C. (2007). Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology 16, 3263–3273.CrossRefGoogle ScholarPubMed
Yohannes, E., Krizanauskiene, A., Valcu, M., Bensch, S. and Kempenaers, B. (2009). Prevalence of malaria and related haemosporidian parasites in two shorebird species with different winter habitat distribution. Journal of Ornithology 150, 287–291.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