Skip to main content Accessibility help
×
Home

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

  • DIANA C. OUTLAW (a1) and ROBERT E. RICKLEFS (a2)

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.

Copyright

Corresponding author

* Corresponding author: Department of Biological Sciences, Mississippi State University, Mississippi State, MS 39759, USA. E-mail: doutlaw@biology.msstate.edu

References

Hide All
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, 684689.
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, 29352944.
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, 15831589.
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.
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.
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, 363369.
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, 311.
Drummond, A. J. and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.
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, 1137311377.
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, 967980.
Forney, L. J., Zhou, X. and Brown, C. J. (2004). Molecular microbial ecology: land of the one-eyed king. Current Opinion in Microbiology 7, 210220.
Garnham, P. C. C. (1966). Malaria Parasites and Other Haemosporidia. Blackwell Scientific Publications, Oxford.
Hellgren, O. (2005). The occurrence of haemosporidian parasites in the Fennoscandian bluethroat (Luscinia svecica) population. Journal of Ornithology 146, 5560.
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, 889896.
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, 747760.
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.
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, 17411750.
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, 709715.
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, 847854.
Librado, P. and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 14511452.
Littlewood, D. T. J. (2012). Systematics as a cornerstone of parasitology: overview and preface. Parasitology 138, 16331637.
Liu, L. (2008). BEST: Bayesian estimation of species trees under the coalescent model. Bioinformatics 24, 25422543.
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.
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, 261273.
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.
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, 388397.
Morrison, D. A. (2009). Evolution of the Apicomplexa: where are we now? Trends in Parasitology 25, 375382.
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, 275280.
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, 103107.
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, 453464.
Pérez-Tris, J., Hasselquist, D., Hellgren, O., Krizanauskiene, A., Waldenström, J. and Bensch, S. (2005). What are malaria parasites? Trends in Parasitology 21, 209211.
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, 23452350.
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, 7483.
Perkins, S. L., Martinsen, E. S. and Falk, B. G. (2011). Do molecules matter more than morphology? Promises and pitfalls in parasites. Parasitology 138, 16641674.
Ramiro, R. S., Reece, S. E. and Obbard, D. J. (2012). Molecular evolution and phylogenetics of rodent malaria parasites. BMC Evolutionary Biology 12, 219.
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, 1490214907.
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, 885892.
Ricklefs, R. E. and Outlaw, D. C. (2010). A molecular clock for malaria parasites. Science 329, 226229.
Ricklefs, R. E., Fallon, S. M. and Bermingham, E. (2004). Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Systematic Biology 53, 111119.
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, 543559.
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, 375379.
Sibley, C. G. and Ahlquist, J. E. (1990). Phylogeny and Classification of Birds. Yale University Press, New Haven, CT, USA.
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, 147.
Telford, S. R. (2009). Hemoparasites of the Reptilia. CRC Press, Boca Raton, FL, USA.
Valkiūnas, G. (2005). Avian Malaria Parasites and Other Haemosporidia. CRC Press, Boca Raton, FL, USA.
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, 15121515.
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, 10611077.
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, 170177.
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, 231232.
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.
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, 697703.
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, 657665.

Keywords

Type Description Title
WORD
Supplementary materials

Outlaw and Ricklefs Supplementary Material
Tables and Figure

 Word (1.1 MB)
1.1 MB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed