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Linkage between mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites, with a description of Plasmodium (Novyella) ashfordi sp. nov

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Abstract

Numerous lineages of avian malaria parasites of the genus Plasmodium have been deposited in GenBank. However, only seven morphospecies have been linked to these lineages. This study linked two molecular sequences with morphospecies of malaria parasites. Two species of Plasmodium (mitochondrial cytochrome b gene lineages P-GRW2 and P-GRW4) were isolated from naturally infected adult great reed warblers (Acrocephalus arundinaceus) and inoculated to naive juvenile individuals of the same host species. Heavy parasitemia developed in the subinoculated birds, which enable identification of the species and deposition of their voucher specimens. Parasites of the lineage P-GRW2 were described as a new species, Plasmodium (Novyella) ashfordi, which is characterized primarily by the fan-like mature erythrocytic meronts containing seven to eight merozoites and the terminal position of clumped pigment granules in the gametocytes. Illustrations of the blood stages of the new species and Plasmodium (Haemamoeba) relictum (lineage P-GRW4) are given. The parasites of both lineages are transmitted in Africa and probably not in northern Europe. Other lineages closely related to P. ashfordi and P. relictum are identified. This study establishes the value of PCR-based identification of avian malaria parasites.

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References

  • Atkinson CT, van Riper C III (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In: Loye JE, Zuk M (eds) Bird–parasite interactions: ecology, evolution, and behaviour, Oxford University Press, Oxford, pp 19–48

    Google Scholar 

  • Atkinson CT, Dusek RJ, Woods KL, Iko WM (2000) Pathogenicity of avian malaria in experimentally-infected Hawaii Amakihi. J Wildl Dis 36:197–204

    PubMed  CAS  Google Scholar 

  • Beadell JS, Gering E, Austin J, Dumbacher JP, Peirce M, Pratt TK, Atkinson CT, Fleischer RC (2004) Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol Ecol 13:3829–3844

    Article  PubMed  Google Scholar 

  • Beadell JS, Ishtiaq F, Covas R, Melo M, Warren BH, Atkinson CT, Bensch S, Graves GR, Jhala YV, Peirce MA, Rahmani AR, Fonseca DM, Fleischer RC (2006) Global phylogeographic limits of Hawaii’s avian malaria. Proc R Soc B 273:2935–2944

    Article  PubMed  Google Scholar 

  • Bensch S, Åkesson S (2003) Temporal and spatial variation of hematozoans in Scandinavian willow warblers. J Parasitol 89:388–391

    Article  PubMed  Google Scholar 

  • Bensch S, Stjernman M, Hasselquist D, Ostman O, Hansson B, Westerdahl H, Pinheiro RT (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proc R Soc Lond B 267:1583–1589

    Article  CAS  Google Scholar 

  • Bensch S, Pérez-Tris J, Waldensrtöm J, Hellgren O (2004) Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution 58:1617–1621

    PubMed  CAS  Google Scholar 

  • Bensch S, Waldenström J, Jonzén N, Westerdahl H, Hansson B, Sejberg D, Hasselquist D (2007) Temporal dynamics and diversity of avian malaria parasites in a single host species. J Anim Ecol 76:112–122

    Article  PubMed  Google Scholar 

  • Bishop MA, Bennett GF (1992) Host–parasite catalogue of the avian haematozoa: supplement 1; Bibliography of the avian blood-inhabiting haematozoa: supplement 2. Mem Univ Newfoundland Occas Pap Biol 15:1–244

    Google Scholar 

  • Bonneaud C, Pérez-Tris J, Federici P, Chastel O, Sorci G (2006) Major histocompatibility alleles associated with local resistance to malaria in a passerine. Evolution 60:383–389

    PubMed  CAS  Google Scholar 

  • Escalante AA, Freeland DE, Collins WE, Lal AA (1998) The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proc Natl Acad Sci USA 95:8124–8129

    Article  PubMed  CAS  Google Scholar 

  • Fallon S, Bermingham E, Ricklefs E (2003) Island and taxon effects in parasitism revisited: avian malaria in the Lesser Antilles. Evolution 57:606–615

    PubMed  Google Scholar 

  • Feldman RA, Freed LA, Cann RL (1995) A PCR test for avian malaria in Hawaiian birds. Mol Ecol 4:663–673

    Article  PubMed  CAS  Google Scholar 

  • Garnham PCC (1966) Malaria parasites and other Haemosporidia. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • Garnham PCC, Duggan AJ (1986) Catalogue of the Garnham collection of malaria parasites and other Haemosporidia. The Wellcome Trust, London

    Google Scholar 

  • Godfrey RD, Fedynich AM, Pence DB (1987) Quantification of hematozoa in blood smears. J Wildl Dis 23:558–565

    PubMed  Google Scholar 

  • Greiner EC, Bennett GF, White EM, Coombs RF (1975) Distribution of the avian hematozoa of North America. Can J Zool 53:1762–1787

    Article  PubMed  CAS  Google Scholar 

  • Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387

    Article  PubMed  CAS  Google Scholar 

  • Hellgren O, Waldenström J, Bensch S (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol 90:797–802

    Article  PubMed  CAS  Google Scholar 

  • Iezhova TA, Valkiūnas G, Barlein F (2005) Vertebrate host specificity of two avian malaria parasites of subgenus Novyella: Plasmodium nucleophilum and Plasmodium vaughani. J Parasitol 91:472–474

    Article  PubMed  Google Scholar 

  • Jarvi SI, Schultz JJ, Atkinson CT (2002) PCR diagnostics underestimate the prevalence of avian malaria (Plasmodium relictum) in experimentally-infected passerines. J Parasitol 88:153–158

    PubMed  Google Scholar 

  • Kilpatrick AM, LaPointe DA, Atkinson CT, Woodworth BL, Lease JK, Reiter ME, Gross K (2006) Effects of chronic avian malaria (Plasmodium relictum) infection on reproductive success of Hawaii Amakihi (Hemignathus virens). Auk 123:764–774

    Article  Google Scholar 

  • Križanauskienė A, Hellgren O, Kosarev V, Sokolov L, Bensch S, Valkiūnas G (2006) Variation in host specificity between species of avian haemosporidian parasites: evidence from parasite morphology and cytochrome b gene sequences. J Parasitol 92:1319–1324

    Article  PubMed  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Laird M, van Riper C (1981) Questionable reports of Plasmodium from birds in Hawaii, with the recognition of P. relictum ssp. capistranoae. In: Canning EV (ed) Parasitological topics. A presentation volume to P. C. C. Garnham on the occasion of his 80th birthday, Special Publication No. 1, Allen, Lawrence, pp 159–165

  • McClure HE, Poonswad P, Greiner EC, Laird M (1978) Haematozoa in the birds of Eastern and Southern Asia. Memorial University of Newfoundland, St. John’s

  • McCutchan TF, Grim KC, Li J, Weiss W, Rathore D, Sullivan M, Graczyk TK, Kumar S, Cranfield MR (2004) Measuring the effects of an ever-changing environment on malaria control. Infect Immun 72:2248–2253

    Article  PubMed  CAS  Google Scholar 

  • Nylander JAA (2004) mrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University. Software available at: http://www.ebc.uu.se/systzoo/staff/nylander.html

  • Pérez-Tris J, Bensch S (2005) Diagnosing genetically diverse avian malaria infections using mixed-sequence analysis and TA-cloning. Parasitology 131:1–9

    Article  CAS  Google Scholar 

  • Perkins SL (2000) Species concepts and malaria parasites: detecting a cryptic species of Plasmodium. Proc R Soc Lond B 267:2345–2350

    Article  CAS  Google Scholar 

  • Perkins SL, Schall JJ (2002) A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. J Parasitol 88:972–978

    PubMed  CAS  Google Scholar 

  • Perkins SL, Osgood SM, Schall JJ (1998) Use of PCR for detection of subpatent infections in lizard malaria: implications for epizootiology. Mol Ecol 7:1587–1590

    Article  CAS  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Rambaut A, Drummond A. TRACER: a program for analysing results from Bayesian MCMC programs such as BEAST & MrBayes. Available at http://evolve.zoo.ox.ac.uk

  • Reullier J, Pérez-Tris J, Bensch S, Secondi J (2006) Diversity, distribution and exchange of blood parasites meeting at an avian moving contact zone. Mol Ecol 15:753–763

    Article  PubMed  Google Scholar 

  • Ricklefs RE, Fallon SM (2002) Diversification and host switching in avian malaria parasites. Proc R Soc Lond B 269:885–892

    Article  Google Scholar 

  • Ricklefs RE, Fallon SM, Bermingham E (2004) Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Syst Biol 53:111–119

    Article  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Russell PF (1932) Avian malaria studies, V. Plasmodium capistrani sp. nov., an avian malaria parasite in the Philippines. Philipp J Sci 48:269–289

    Google Scholar 

  • Schrenzel MD, Maalouf GA, Keener LL, Gaffney PM (2003) Molecular characterisation of malarial parasites in captive passerines birds. J Parasitol 89:1025–1033

    Article  PubMed  CAS  Google Scholar 

  • Sehgal RNM, Jones HI, Smith TB (2005) Blood parasites of some West African birds. J Vet Med Sci 67:295–301

    Article  PubMed  Google Scholar 

  • Unnasch TR, McLafferty M, Wirth DF (1985) The primary structure of the rRNA insertions of Plasmodium lophurae. Mol Biochem Parasitol 16:149–161

    Article  PubMed  CAS  Google Scholar 

  • Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. CRC, Boca Raton

    Google Scholar 

  • Valkiūnas G, Sehgal RNM, Iezhova TA, Smith TB (2005) Further observations on the blood parasites of birds in Uganda. J Wildl Dis 41:580–587

    PubMed  Google Scholar 

  • Valkiūnas G, Bensch S, Iezhova TA, Križanauskienë A, Hellgren O, Bolshakov CV (2006) Nested cytochrome b PCR diagnostics underestimate mixed infections of avian blood hemosporidian parasites: microscopy is still essential. J Parasitol 92:418–422

    Article  PubMed  Google Scholar 

  • van Riper III C, van Riper SG, Goff ML, Laird M (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monogr 56:327–344

    Article  Google Scholar 

  • Waldenström J, Bensch S, Kiboi D, Hasselquist D, Ottosson U (2002) Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Mol Ecol 11:1545–1554

    Article  PubMed  Google Scholar 

  • Waldenström J, Bensch S, Hasselquist D, Östman Ö (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parasitol 90:191–194

    Article  PubMed  Google Scholar 

  • Westerdahl H, Waldenström J, Hansson B, Hasselquist D, von Schantz T, Bensch S (2005) Associations between malaria and MHC genes in a migratory songbird. Proc R Soc Lond B 272:1511–1518

    Article  CAS  Google Scholar 

  • Wiersch SC, Maier WA, Kampen H (2005) Plasmodium (Haemamoeba) cathemerium gene sequences for phylogenetic analysis of malaria parasites. Parasitol Res 96:90–94

    Article  PubMed  CAS  Google Scholar 

  • Wilgenbusch JC, Warren DL, Swofford DL (2004) AWTY: a system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference. Available at: http://ceb.csit.fsu.edu/awty

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Acknowledgements

This article benefited from comments made by John R. Baker. The authors are grateful to Alan Warren, Natural History Museum, London for providing the type material of P. vaughani and P. relictum, and Robert Adlard, Queensland Museum, Queensland for providing the voucher blood slide of P. relictum capistranoae. The present study was supported in part by the Swedish Research Council, Carl Tryggers Foundation, and the Lithuanian State Science and Studies Foundation. The experiments described herein comply with the current laws of Sweden, Bulgaria, and Lithuania.

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Authors and Affiliations

  1. Institute of Ecology, Vilnius University, Akademijos 2, Vilnius 21, LT-08412, Lithuania

    Gediminas Valkiūnas & Tatjana A. Iezhova

  2. Institute of Zoology, Bulgarian Academy of Sciences, Blvd. Tzar Osvoboditel 1, 1000, Sofia, Bulgaria

    Pavel Zehtindjiev & Mihaela Ilieva

  3. Department of Animal Ecology, Ecology Building, Lund University, SE-22362, Lund, Sweden

    Olof Hellgren & Staffan Bensch

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  1. Gediminas Valkiūnas
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  2. Pavel Zehtindjiev
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  4. Mihaela Ilieva
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  5. Tatjana A. Iezhova
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  6. Staffan Bensch
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Correspondence to Gediminas Valkiūnas.

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Valkiūnas, G., Zehtindjiev, P., Hellgren, O. et al. Linkage between mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites, with a description of Plasmodium (Novyella) ashfordi sp. nov. Parasitol Res 100, 1311–1322 (2007). https://doi.org/10.1007/s00436-006-0409-3

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  • DOI: https://doi.org/10.1007/s00436-006-0409-3

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