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Species limits in avian malaria parasites (Haemosporida): how to move forward in the molecular era

Published online by Cambridge University Press:  09 May 2014

DIANA C. OUTLAW  and
ROBERT E. RICKLEFS
DIANA C. OUTLAW*
Affiliation:
Department of Biological Sciences, Mississippi State University, Mississippi State, MS 39759, USA
ROBERT E. RICKLEFS
Affiliation:
Department of Biology, University of Missouri-St. Louis, One University Boulevard, St. Louis, MO 63121, USA
*
*Corresponding author: Department of Biological Sciences, Mississippi State University, Mississippi State, MS 39759, USA. E-mail: doutlaw@biology.msstate.edu
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Summary

Delimiting species of malaria parasites (Haemosporida) has become increasingly problematic as new lineages of parasites are identified solely by molecular information, particularly mitochondrial cytochrome b sequence data. In this review, we highlight some of the issues, both historical and contemporary, that have hindered the development of objective criteria to diagnose, delimit and define species of haemosporidians. Defining species is not the focal interest of most researchers, most of whom merely wish to determine whether lineages identified in their samples match those of other researchers, and if so, where and in which host species. Rather than revisiting all the issues with respect to delimiting and naming species, we instead focus on finding a practical near-term resolution to the ‘species problem’ that utilizes the community's largest resource: mitochondrial cytochrome b DNA sequences. We recommend a standardized procedure to ‘tag’ these sequences, based on per cent sequence similarity, that will allow researchers to directly assess the novelty, known hosts and geographic distribution of avian malaria parasite lineages.

Keywords

Avian malariaspecies limitsHaemosporida
Type
Review Article
Information
Parasitology , Volume 141 , Issue 10 , September 2014 , pp. 1223 - 1232
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Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Adl, S. M., Leander, B. S., Simpson, A. G. B., Archibald, J. M., Anderson, O. R., Bass, D., Bowser, S. S., Brugerolle, G., Farmer, M. A., Karpov, S., Kolisko, M., Lane, C. E., Lodge, D. J., Mann, D. G., Meisterfeld, R., Mendoza, L., Moestrup, Ø., Mozley-Standridge, S. E., Smirnov, A. V. and Spiegel, F. (2007). Diversity, nomenclature, and taxonomy of protists. Systematic Biology 56, 684–689.CrossRefGoogle ScholarPubMed
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 Series B 273, 2935–2944.Google ScholarPubMed
Bensch, S., Stjernman, M., Hasselquist, D., Östman, Ö., 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 Series B 267, 1583–1589.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, 1617–1621.Google 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, 1353–1358.CrossRefGoogle ScholarPubMed
Bensch, S., Hellgren, O., Krizanaskiene, A., Palinauskas, V., Valkiūnas, G., Outlaw, D. C. and Ricklefs, R. E. (2013). How can we determine the molecular clock of malaria parasites? Trends in Parasitology 29, 363–369.CrossRefGoogle ScholarPubMed
Braga, É. M., Silveira, P., Belo, N. O. and Valkiūnas, G. (2011). Recent advances in the study of avian malaria: an overview with an emphasis on the distribution of Plasmodium spp. in Brazil. Memórias do Instituto Oswaldo Cruz 106, 3–11.CrossRefGoogle Scholar
Drummond, A. J. and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.CrossRefGoogle ScholarPubMed
Escalante, A. A. and Ayala, F. J. (1994). Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. Proceedings of the National Academy of Sciences USA 91, 11373–11377.Google Scholar
Falk, B. G., Mahler, D. L. and Perkins, S. L. (2011). Tree-based delimitation of morphologically ambiguous taxa: a study of the lizard malaria parasites on the Caribbean island of Hispaniola. International Journal of Parasitology 41, 967–980.CrossRefGoogle ScholarPubMed
Forney, L. J., Zhou, X. and Brown, C. J. (2004). Molecular microbial ecology: land of the one-eyed king. Current Opinion in Microbiology 7, 210–220.Google Scholar
Garnham, P. C. C. (1966). Malaria Parasites and Other Haemosporidia. Blackwell Scientific Publications, Oxford.Google Scholar
Hellgren, O. (2005). The occurrence of haemosporidian parasites in the Fennoscandian bluethroat (Luscinia svecica) population. Journal of Ornithology 146, 55–60.Google Scholar
Hellgren, O., Krizanauskiene, A., Valkiūnas, G. and Bensch, S. (2007). Diversity and phylogeny of mitochondrial cytochrome b lineages from six morphological species of avian Haemoproteus . Journal of Parasitology 93, 889–896.Google Scholar
Hey, J. (2009). https://bio.cst.temple.edu/~hey/program_files/IM/Introduction_to_IM_and_IMa_3_5_2007.pdf.Google Scholar
Hey, J. and Nielsen, R. (2004). Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis . Genetics 167, 747–760.Google Scholar
Ishak, H. D., Dumbacher, J. P., Anderson, N. L., Keane, J. J., Valkiūnas, G., Haig, S. M., Tell, L. A. and Sehgal, R. N. M. (2008). Blood parasites in owls with conservation implications for the spotted owl (Strix occidentalis). PLoS One 3, e2304.Google Scholar
Jarvi, S. I., Farias, M. E., Lapointe, D. A., Belcaid, M. and Atkinson, C. T. (2013). Next-generation sequencing reveals cryptic mtDNA diversity of Plasmodium relictum in the Hawaiian Islands. Parasitology 140, 1741–1750.Google Scholar
Krone, O., Waldenström, J., Valkiūnas, G., Lessow, O., Muller, K., Iezhova, T. A., Fickel, J. and Bensch, S. (2008). Haemosporidian blood parasites in European birds of prey and owls. Journal of Parasitology 94, 709–715.Google Scholar
Levin, I. I., Valkiunas, G., Iezhova, T. A., O'Brien, S. L. and Parker, P. G. (2012). Novel Haemoproteus species (Haemosporida: Haemoproteidae) from the Swallow-Tailed Gull (Lariidae), with remarks on the host range of Hippoboscid-transmitted avian hemoproteids. Journal of Parasitology 98, 847–854.Google Scholar
Librado, P. and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.Google Scholar
Littlewood, D. T. J. (2012). Systematics as a cornerstone of parasitology: overview and preface. Parasitology 138, 1633–1637.Google Scholar
Liu, L. (2008). BEST: Bayesian estimation of species trees under the coalescent model. Bioinformatics 24, 2542–2543.Google Scholar
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, 279–288.CrossRefGoogle ScholarPubMed
Martinsen, E. S., Perkins, S. L. 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 4, 261–273.CrossRefGoogle Scholar
Marzal, A., Ricklefs, R. E., Valkiūnas, G., Albayrak, T., Arriero, E., Bonneaud, C., Czirjak, G. A., Ewen, J., Hellgren, O., Horakova, D., Iezhova, T. A., Jensen, H., Krizanauskiene, A., Lima, M. R., de Lope, F., Magnussen, E., Martin, L. B., Moller, A. P., Palinauskas, B., Pap, P. L., Pérez-Tris, J., Sehgal, R. N. M., Soler, M., Szöllosi, E., Westerdahl, H., Zetindjiev, P. and Bensch, S. (2011). Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS One 6, e21905.Google Scholar
Merino, S., Hennicke, J., Martínez, J., Ludynia, K., Torres, R., Work, T. M., Stroud, S., Masello, J. F. and Quillfeldt, P. (2012). Infection by Haemoproteus parasites in four species of frigatebirds and the description of a new species of Haemoproteus (Haemosporida: Haemoproteidae). Journal of Parasitology 98, 388–397.Google Scholar
Morrison, D. A. (2009). Evolution of the Apicomplexa: where are we now? Trends in Parasitology 25, 375–382.CrossRefGoogle ScholarPubMed
Palinauskas, V., Krizanauskiene, A., Iezhova, T. A. and Bolshakov, C. V. (2013). A new method for isolation of purified genomic DNA from haemosporidian parasites inhabiting nucleated red blood cells. Experimental Parasitology 133, 275–280.CrossRefGoogle ScholarPubMed
Paperna, I. and Yosef, R. (2010). Description of a new species of Haemoproteus (Haemosporidia, Apicomplexa) from an Orange-tufted Sunbird Nectarinia osea . Acta Parasitologica 55, 103–107.CrossRefGoogle Scholar
Pérez-Ponce de Léon, G. and Nadler, S. A. (2010). What we won't recognize can hurt us: a plea for awareness about cryptic species. Journal of Parasitology 96, 453–464.CrossRefGoogle Scholar
Pérez-Tris, J., Hasselquist, D., Hellgren, O., Krizanauskiene, A., Waldenström, J. and Bensch, S. (2005). What are malaria parasites? Trends in Parasitology 21, 209–211.Google Scholar
Perkins, S. L. (2000). Species concept and malaria parasites: detecting a cryptic species of Plasmodium . Proceedings of the Royal Society, Series B: Biological Sciences 267, 2345–2350.Google Scholar
Perkins, S. L., Sarkar, I. N. and Carter, R. (2007). The phylogeny of rodent malaria parasites: simultaneous analysis across three genomes. Infection, Genetics and Evolution 7, 74–83.CrossRefGoogle ScholarPubMed
Perkins, S. L., Martinsen, E. S. and Falk, B. G. (2011). Do molecules matter more than morphology? Promises and pitfalls in parasites. Parasitology 138, 1664–1674.Google Scholar
Ramiro, R. S., Reece, S. E. and Obbard, D. J. (2012). Molecular evolution and phylogenetics of rodent malaria parasites. BMC Evolutionary Biology 12, 219.CrossRefGoogle ScholarPubMed
Rich, S. M., Leendertz, F. H., Xu, G., LeBreton, M., Djoko, C. F., Aminake, M. N., Takang, E. E., Diffo, J. L. D., Pike, B. L., Rosenthal, B. M., Formenty, P., Boesch, C., Ayala, F. J. and Wolfe, N. D. (2009). The origin of malignant malaria. Proceedings of the National Academy of Sciences USA 106, 14902–14907.Google Scholar
Ricklefs, R. E. and Fallon, S. M. (2002). Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society of London, Series B 269, 885–892.Google Scholar
Ricklefs, R. E. and Outlaw, D. C. (2010). A molecular clock for malaria parasites. Science 329, 226–229.Google Scholar
Ricklefs, R. E., Fallon, S. M. and Bermingham, E. (2004). Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Systematic Biology 53, 111–119.Google Scholar
Ricklefs, R. E., Swanson, B., Fallon, S. M., Martinez, A., Scheuerlein, A., Gray, J. and Latta, S. L. (2005). Community relationships of avian malaria parasites in southern Missouri. Ecological Monographs 75, 543–559.CrossRefGoogle Scholar
Sehgal, R. N. M., Hull, A. C., Anderson, N. L., Valkiunas, G., Markovets, M. J., Kawamura, S. and Tell, L. A. (2006). Evidence for cryptic speciation of Leucocytozoon spp. (Haemosporida, Leucocytozoidae) in diurnal raptors. Journal of Parasitology 92, 375–379.Google Scholar
Sibley, C. G. and Ahlquist, J. E. (1990). Phylogeny and Classification of Birds. Yale University Press, New Haven, CT, USA.Google Scholar
Svensson-Coelho, M., Blake, J. G., Loiselle, B. A., Penrose, A. S., Parker, P. G. and Ricklefs, R. E. (2013). Diversity, prevalence, and host specificity of avian Plasmodium and Haemoproteus in a western Amazon assemblage. Ornithological Monographs 76, 1–47.Google Scholar
Telford, S. R. (2009). Hemoparasites of the Reptilia. CRC Press, Boca Raton, FL, USA.Google Scholar
Valkiūnas, G. (2005). Avian Malaria Parasites and Other Haemosporidia. CRC Press, Boca Raton, FL, USA.Google Scholar
Valkiūnas, G., Iezhova, T. A., Loiseau, C. and Sehgal, R. (2009 a). Nested cytochrome b polymerase chain reaction diagnostics detect sporozoites of hemosporidian parasites in peripheral blood of naturally infected birds. Journal of Parasitology 95, 1512–1515.Google Scholar
Valkiūnas, G., Iezhova, T. A., Loiseau, C., Smith, T. B. and Sehgal, R. N. M. (2009 b). New malaria parasites of the subgenus Novyella in African rainforest birds, with remarks on their high prevalence, classification and diagnostics. Parasitology Research 104, 1061–1077.Google Scholar
Valkiūnas, G., Sehgal, R. N., Iezhova, T. A. and Hull, A. C. (2010). Identification of Leucocytozoon toddi group (Haemosporida: Leucocytozoidae), with remarks on the species taxonomy of leucocytozoids. Journal of Parasitology 96, 170–177.Google Scholar
Valkiūnas, G., Ashford, R. W., Bensch, S., Killick-Kendrick, R. and Perkins, S. (2011). A cautionary note concerning Plasmodium in apes. Trends in Parasitology 27, 231–232.Google Scholar
Wang, B., Ekblom, R., Castoe, T. A., Jones, E. P., Kozma, R., Bongcam-Rudloff, E., Pollock, D. D. and Höglund, J. (2012). Transcriptome sequencing of black grouse (Tetrao tetrix) for immune gene discovery and microsatellite development. Open Biology 2, 120054. http://dx.doi.org/10.1098/rsob.120054.Google Scholar
Weisburg, W. G., Barns, S. M., Pelletier, D. A. and Lane, D. J. (1991). 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology 173, 697–703.Google Scholar
Zehtindjiev, P., Križanauskienė, A., Bensch, S., Palinauskas, V., Asghar, M., Dimitrov, D., Scebba, S. and Valkiūnas, G. (2012). A new morphologically distinct avian malaria parasite that fails detection by established polymerase chain reaction-based protocols for amplification of the cytochrome b gene. Journal of Parasitology 98, 657–665.Google Scholar
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