Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-23T03:29:27.808Z Has data issue: false hasContentIssue false
  • English
  • Français

The rediscovery of malaria parasites of ungulates

Published online by Cambridge University Press:  22 July 2016

THOMAS J. TEMPLETON ,
ELLEN MARTINSEN ,
MORAKOT KAEWTHAMASORN  and
OSAMU KANEKO
THOMAS J. TEMPLETON
Affiliation:
Department of Protozoology, Institute of Tropical Medicine (NEKKEN), Nagasaki University, 1-12-4 Sakamoto, Nagasaki 852-8523, Japan Department of Microbiology and Immunology, Weill Cornell Medical School, New York, New York 10021, USA
ELLEN MARTINSEN
Affiliation:
Center for Conservation and Evolutionary Genetics, Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC 20013-7012, USA
MORAKOT KAEWTHAMASORN
Affiliation:
The Veterinary Parasitology Unit, Department of Pathology, Faculty of Veterinary Science, Chulalongkorn University, Bangkok 10330, Thailand
OSAMU KANEKO*
Affiliation:
Department of Protozoology, Institute of Tropical Medicine (NEKKEN), Nagasaki University, 1-12-4 Sakamoto, Nagasaki 852-8523, Japan
*
*Corresponding author: Department of Protozoology, Institute of Tropical Medicine (NEKKEN), Nagasaki University, 1-12-4 Sakamoto, Nagasaki 852-8523, Japan. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Over a hundred years since their first description in 1913, the sparsely described malaria parasites (genus Plasmodium) of ungulates have been rediscovered using molecular typing techniques. In the span of weeks, three studies have appeared describing the genetic characterization and phylogenetic analyses of malaria parasites from African antelope (Cephalophus spp.) and goat (Capra aegagrus hircus), Asian water buffalo (Bubalus bubalis), and North American white-tailed deer (Odocoileus virginianus). Here we unify the contributions from those studies with the literature on pre-molecular characterizations of ungulate malaria parasites, which are largely based on surveys of Giemsa-reagent stained blood smears. We present a phylogenetic tree generated from all available ungulate malaria parasite sequence data, and show that parasites from African duiker antelope and goat, Asian water buffalo and New World white-tailed deer group together in a clade, which branches early in Plasmodium evolution. Anopheline mosquitoes appear to be the dominant, if not sole vectors for parasite transmission. We pose questions for future phylogenetic studies, and discuss topics that we hope will spur further molecular and cellular studies of ungulate malaria parasites.

Keywords

malariaungulatesruminantsHaemosporidiaApicomplexamalaria parasites
Type
Review Article
Information
Parasitology , Volume 143 , Issue 12 , October 2016 , pp. 1501 - 1508
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

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

Arai, S., Tsuji, M., Kim, S. J., Nakada, K., Kirisawa, R., Ohta, M. and Ishihara, C. (1998). Antigenic and genetic diversities of Babesia ovata in persistently infected cattle. Journal of Veterinary Medicine and Science 60, 1321–1327.CrossRefGoogle ScholarPubMed
Ayouba, A., Mouacha, F., Learn, G. H., Mpoudi-Ngole, E., Rayner, J. C., Sharp, P. M., Hahn, B. H., Delaporte, E. and Peeters, M. (2012). Ubiquitous Hepatocystis infections, but no evidence of Plasmodium falciparum-like malaria parasites in wild greater spot-nosed monkeys (Cercopithecus nictitans). International Journal of Parasitology 42, 709–713.CrossRefGoogle ScholarPubMed
Bensch, S., Canbäck, B., DeBarry, J. D., Johansson, T., Hellgren, O., Kissinger, J. C., Palinauskas, V., Videvall, E. and Valkiūnas, G. (2016). The genome of Haemoproteus tartakovskyi and its relationship to human malaria parasites. Genome Biology and Evolution 8, 1361–1373.CrossRefGoogle ScholarPubMed
Borner, J., Pick, C., Thiede, J., Kolawole, O. M., Kingsley, M. T., Schulze, J., Cottontail, V. M., Wellinghausen, N., Schmidt-Chanasit, J., Bruchhaus, I. and Burmester, T. (2016). Phylogeny of haemosporidium blood parasites revealed by a multi-gene approach. Molecular Phylogenetics and Evolution 94, 221–231.CrossRefGoogle ScholarPubMed
Boundenga, L., Makanga, B., Ollomo, B., Gilabert, A., Rougeron, V., Mve-Ondo, B., Arnathau, C., Durand, P., Moukodoum, N. D., Okouga, A. P., Delicat-Loembet, L., Yacka-Mouele, L., Rahola, N., Leroy, E., Ba, C. T., Renaud, F., Prugnolle, F. and Paupy, C. (2016). Haemosporidian parasites of antelopes and other vertebrates from Gabon, Central Africa. PLoS ONE 11, e0148958.CrossRefGoogle ScholarPubMed
Bruce, D., Harvey, D., Hamerton, A. E. and Bruce, L. (1913). Plasmodium cephalophi sp. nov . Proceedings of the Royal Society B 87, 45–47.Google Scholar
Bruce, D., Harvey, D., Hammerton, A. E., Davey, J. B. and Bruce, L. (1915). Trypanosomes and other parasites of animals in Nyasaland. Reports of the Sleeping Sickness Commission of the Royal Society 16, 203–208.Google Scholar
de Mello, F. and Paes, S. (1923). Sur une plasmodie du sang des chèvres. Comptes Rendus des Séances de la Société de Biologie 88, 829–830.Google Scholar
Dissanaike, A. S. (1963). On some blood parasites of wild animals in Ceylon. Ceylon Veterinary Journal 11, 73–86.Google Scholar
Escalante, A. A., Freeland, D. E., Collins, W. E. and Lal, A. A. (1998). The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proceedings of the National Academy of Sciences of the United States of America 95, 8124–8129.CrossRefGoogle ScholarPubMed
Garnham, P. C. C. (1958). A malaria parasite of the hippopotamus. Journal of Protozoology 5, 149–151.CrossRefGoogle Scholar
Garnham, P. C. C. (1966). Malaria Parasites and other Haemosporidia. Blackwell Sci. Pub., Oxford.Google Scholar
Garnham, P. C. C. and Edeson, J. F. B. (1962). Two new malaria parasites of the Malayan mouse deer. Rivista di Malariologia 41, 1–8.Google Scholar
Garnham, P. C. C. and Kuttler, K. L. (1980). A malaria parasite of the white-tailed deer (Odocoileus virginianus) and its relation with known species of Plasmodium in other ungulates. Proceedings of the Royal Society of London B Biological Sciences 206, 395–402.Google ScholarPubMed
Godfray, H. C., Beddington, J. R., Crute, I. R., Haddad, L., Lawrence, D., Muir, J. F., Pretty, J., Robinson, S., Thomas, S. M. and Toulmin, C. (2010). Food security: the challenge of feeding 9 billion people. Science 327, 812–818.CrossRefGoogle ScholarPubMed
Keymer, I. F. (1966). Studies on Plasmodium (Vinckeia) cephalophi of the grey duiker (Sylvicapra grimmia). Annals of Tropical Medicine and Parasitology 60, 129–138.CrossRefGoogle ScholarPubMed
Keymer, I. F. (1969). Investigations on the duiker (Sylvicapra grimmia) and its blood protozoa in Central Africa. Philosophical Transactions of the Royal Society of London B Biological Sciences 255, 33–108.Google Scholar
Kolte, S. W., Maske, D. K. and Tekade, S. R. (2002). A note on occurrence of Plasmodium bubalis in buffaloes (Bubalus bubalis) at Nagpur. Journal of Veterinary Parasitology 16, 193.Google Scholar
Kuttler, K. L., Robinson, R. M. and Rogers, W. P. (1967). Exacerbation of latent erythrocytic infections in deer following splenectomy. Canadian Journal of Comparative Medicine and Veterinary Science 31, 317–319.Google 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 47, 261–273.CrossRefGoogle ScholarPubMed
Martinsen, E. S., McInerney, N., Brightman, H., Ferebee, K., Walsh, T., McShea, W. J., Forrester, T. D., Ware, L., Joyner, P. H., Perkins, S. L., Latch, E. K., Yabsley, M. J., Schall, J. J. and Fleischer, R. C. (2016). Hidden in plain sight: Cryptic and endemic malaria parasites in North American white-tailed deer (Odocoileus virginianus). Science Advances 2, e1501486.CrossRefGoogle ScholarPubMed
Okell, L. C., Ghani, A. C., Lyons, E. and Drakeley, C. J. (2009). Submicroscopic infection in Plasmodium falciparum-endemic populations: a systematic review and meta-analysis. Journal of Infectious Disease 200, 1509–1517.CrossRefGoogle ScholarPubMed
Oyola, S. O., Manske, M., Campino, S., Claessens, A., Hamilton, W. L., Kekre, M., Drury, E., Mead, D., Gu, Y., Miles, A., MacInnis, B., Newbold, C., Berriman, M. and Kwiatkowski, D. P. (2014). Optimized whole-genome amplification strategy for extremely AT-biased template. DNA Research 21, 661–671.CrossRefGoogle ScholarPubMed
Perkins, S. L. and Schall, J. J. (2002). A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. Journal of Parasitology 88, 972–978.CrossRefGoogle ScholarPubMed
Rao, M. A. N. (1938). A note on Plasmodium bubalis Sheather, 1919. Indian Journal of Veterinary Science and Animal Husbandry 8, 387–389.Google Scholar
Riaz-ul-Hassan, S. (1953). Further observations on malaria in buffaloes. Pakistan Journal of Health 3, 59–63.Google ScholarPubMed
Sandosham, A. A., Eyles, D. E., Wharton, R. G., Warren, M. and Hoo, C. C. (1962). Plasmodium sp. and Hepatocystis sp. in the mouse-deer (Tragulus javanicus) in Malaya. The Medical Journal of Malaya 17, 78–90.Google Scholar
Schaer, J., Perkins, S. L., Decher, J., Leendertz, F. H., Fahr, J., Weber, N. and Matuschewski, K. (2013). High diversity of West African bat malaria parasites and a tight link with rodent Plasmodium taxa. Proceedings of the National Academy of Sciences of the United States of America 110, 17415–17419.CrossRefGoogle Scholar
Shastri, S. R., Shastri, U. V. and Deshpande, P. D. (1985). Haematozoan infections in buffalo, Bubalus bubalis, in Maharashtra. Indian Journal of Parasitology 9, 183–185.Google Scholar
Sheather, A. L. (1919). A malarial parasite in the blood of a buffalo. Journal of Comparative Pathology and Therapeutics 32, 223–229.CrossRefGoogle Scholar
Shinde, P. N., Maske, D. K., Samradhni, D., Kolte, S. W. and Banubakode, S. B. (2005). Some observations on bovine malaria associated with developing phases of Plasmodium bubalis in Vidarbha region of Maharashtra. Journal of Veterinary Parasitology 19, 61–62.Google Scholar
Sundararaman, S. A., Plenderleith, L. J., Liu, W., Loy, D. E., Learn, G. H., Li, Y., Shaw, K. S., Ayouba, A., Peeters, M., Speede, S., Shaw, G. M., Bushman, F. D., Brisson, D., Rayner, J. C., Sharp, P. M. and Hahn, B. H. (2016). Genomes of cryptic chimpanzee Plasmodium species reveal key evolutionary events leading to human malaria. Nature Communications 7, 11078.CrossRefGoogle ScholarPubMed
Templeton, T. J., Asada, M., Jiratanh, M., Ishikawa, S. A., Tiawsirisup, S., Sivakumar, T., Namangala, B., Takeda, M., Mohkaew, K., Ngamjituea, S., Inoue, N., Sugimoto, C., Inagaki, Y., Suzuki, Y., Yokoyama, N., Kaewthamasorn, M. and Kaneko, O. (2016). Ungulate malaria parasites. Scientific Reports 6, 23230.CrossRefGoogle ScholarPubMed
Toumanoff, C. (1939). Le paludisme des buffles peut-il fausser les indices oocystiques et sporozoitiques en Indochine? Bulletin de la Société de Pathologie Exotique et de ses Filiales 32, 80–87.Google Scholar
Valkiūnas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, FL.Google Scholar
van den Berghe, L. (1937). Plasmodium limnotragi n. sp., d'une antilope Limnotragus spekei . Bulletin de la Société de Pathologie Exotique et de ses Filiales 30, 272–274.Google Scholar
Warren, M., Bennett, G. F., and Cheong, W. H. (1964). Natural plasmodial infections in Mansonia (Coquillettidia) crassipes . The Medical Journal of Malaya 19, 55.Google Scholar
Wharton, R. H., Eyles, D. E., Warren, M., Moorhouse, D. E. and Sandosham, A. A. (1963). Investigations leading to the identification of members of the Anopheles umbrosus group as the probable vectors of mouse deer malaria. Bulletin of the World Health Organization 29, 357–374.Google Scholar
Witsenburg, F., Salamin, N. and Christe, P. (2012). The evolutionary host switches of Polychromophilus: a multi-gene phylogeny of the bat malaria genus suggests a second invasion of mammals by a haemosporidian parasite. Malaria Journal 11, 53.CrossRefGoogle ScholarPubMed