Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-24T02:57:17.182Z Has data issue: false hasContentIssue false
  • English
  • Français

Geographic distribution of Theileria sp. (buffalo) and Theileria sp. (bougasvlei) in Cape buffalo (Syncerus caffer) in southern Africa: implications for speciation

Published online by Cambridge University Press:  07 November 2013

RONEL PIENAAR ,
ABDALLA A. LATIF ,
ORIEL M. M. THEKISOE  and
BEN J. MANS
RONEL PIENAAR
Affiliation:
Parasites, Vectors and Vector-Borne Diseases, Agricultural Research Council-Onderstepoort Veterinary Institute, Onderstepoort 0110, South Africa Parasitology Research Programme, Department of Zoology and Entomology, University of the Free State Qwaqwa Campus, Private Bag X13, Phuthaditjhaba 9866, South Africa
ABDALLA A. LATIF
Affiliation:
Parasites, Vectors and Vector-Borne Diseases, Agricultural Research Council-Onderstepoort Veterinary Institute, Onderstepoort 0110, South Africa Department of Veterinary Tropical Diseases, University of Pretoria, Pretoria, South Africa
ORIEL M. M. THEKISOE
Affiliation:
Parasitology Research Programme, Department of Zoology and Entomology, University of the Free State Qwaqwa Campus, Private Bag X13, Phuthaditjhaba 9866, South Africa
BEN J. MANS*
Affiliation:
Parasites, Vectors and Vector-Borne Diseases, Agricultural Research Council-Onderstepoort Veterinary Institute, Onderstepoort 0110, South Africa Department of Veterinary Tropical Diseases, University of Pretoria, Pretoria, South Africa Department of Life and Consumer Sciences, University of South Africa, South Africa
*
* Corresponding author: Parasites, Vectors and Vector-Borne Diseases, Agricultural Research Council-Onderstepoort Veterinary Institute, Onderstepoort 0110, South Africa. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Strict control measures apply to movement of buffalo in South Africa including testing for Theileria parva, the causative agent of Corridor disease in cattle. The official test is a real-time hybridization PCR assay that amplifies the 18S rRNA V4 hyper-variable region of T. parva, T. sp. (buffalo) and T. sp. (bougasvlei). Mixed infections with the latter organisms affect diagnostic sensitivity due to PCR suppression. While the incidence of mixed infections in the Corridor disease endemic region of South Africa is significant, little information is available on the specific distribution and prevalence of T. sp. (buffalo) and T. sp. (bougasvlei). Specific real-time PCR assays were developed and a total of 1211 samples known to harbour these parasites were screened. Both parasites are widely distributed in southern Africa and the incidence of mixed infections with T. parva within the endemic region is similar (∼25–50%). However, a significant discrepancy exists in regard to mixed infections of T. sp. (buffalo) and T. sp. (bougasvlei) (∼10%). Evidence for speciation between T. sp. (buffalo) and T. sp. (bougasvlei) is supported by phylogenetic analysis of the COI gene, and their designation as different species. This suggests mutual exclusion of parasites and the possibility of hybrid sterility in cases of mixed infections.

Keywords

DiagnosticsMixed infectionsPCR suppressionreal-time hybridizationTheileria parvaTheileria sp. (buffalo)Theileria sp. (bougasvlei)speciation
Type
Research Article
Information
Parasitology , Volume 141 , Issue 3 , March 2014 , pp. 411 - 424
Check for updates
Copyright
Copyright © Cambridge University Press 2013 

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

Alfaro, M. E., Zoller, S. and Lutzoni, F. (2003). Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Molecular Biology and Evolution 20, 255–266.Google Scholar
Allsopp, B. A., Baylis, H. A., Allsopp, M. T. P. E., Cavalier-Smith, T., Bishop, R. P., Carrington, D. M., Sohanpal, B. and Spooner, P. (1993). Discrimination between six species of Theileria using oligonucleotide probes which detect small subunit ribosomal RNA sequences. Parasitology 107, 157–165.Google Scholar
Allsopp, M. T., Theron, J., Coetzee, M. L., Dunsterville, M. T. and Allsopp, B. A. (1999). The occurrence of Theileria and Cowdria parasites in African buffalo (Syncerus caffer) and their associated Amblyomma hebraeum ticks. Onderstepoort Journal of Veterinary Research 66, 245–249.Google Scholar
Bishop, R., Musoke, A., Morzaria, S., Gardner, M. and Nene, V. (2004). Theileria: intracellular protozoan parasites of wild and domestic ruminants transmitted by ixodid ticks. Parasitology 129(Suppl.), S271–S283.CrossRefGoogle ScholarPubMed
Chae, J. S., Allsopp, B. A., Waghela, S. D., Park, J. H., Kakuda, T., Sugimoto, C., Allsopp, M. T., Wagner, G. G. and Holman, P. J. (1999). A study of the systematics of Theileria spp. based upon small-subunit ribosomal RNA gene sequences. Parasitology Research 85, 877–883.Google Scholar
Chaisi, M. E., Sibeko, K. P., Collins, N. E., Potgieter, F. T. and Oosthuizen, M. C. (2011). Identification of Theileria parva and Theileria sp. (buffalo) 18S rRNA gene sequence variants in the African Buffalo (Syncerus caffer) in southern Africa. Veterinary Parasitology 182, 150–162.Google Scholar
Conrad, P. A., Stagg, D. A., Grootenhuis, J. G., Irvin, A. D., Newson, J., Njamunggeh, R. E., Rossiter, P. B. and Young, A. S. (1987). Isolation of Theileria parasites from African buffalo (Syncerus caffer) and characterization with anti-schizont monoclonal antibodies. Parasitology 94, 413–423.Google Scholar
Coyne, J. A. and Orr, H. A. (2004). Speciation. Sinauer Associates, Inc., Sunderland, MA, USA.Google Scholar
Cross, P. C., Lloyd-Smith, J. O. and Getz, W. M. (2005). Disentangling association patterns in fission–fusion societies using African buffalo as an example. Animal Behavior 69, 499–506.Google Scholar
Dib, L., Bitam, I., Tahri, M., Bensouilah, M. and De Meeûs, T. (2008). Competitive exclusion between piroplasmosis and anaplasmosis agents within cattle. PLoS Pathogens 4, e7.Google Scholar
El-Sherry, S., Ogedengbe, M. E., Hafeez, M. A. and Barta, J. R. (2013). Divergent nuclear 18S rDNA paralogs in a turkey coccidium, Eimeria meleagrimitis, complicate molecular systematics and identification. International Journal for Parasitology 43, 679–685.Google Scholar
Gou, H., Guan, G., Liu, A., Ma, M., Xu, Z., Liu, Z., Ren, Q., Li, Y., Yang, J., Chen, Z., Yin, H. and Luo, J. (2012). A DNA barcode for Piroplasmea. Acta Tropica 124, 92–97.Google Scholar
Gubbels, M. J., Hong, Y., van der Weide, M., Qi, B., Nijman, I. J., Guangyuan, L. and Jongejan, F. (2000). Molecular characterisation of the Theileria buffeli/orientalis group. International Journal for Parasitology 30, 943–952.Google Scholar
Halley, D. J., Vandewalle, M. E. J., Mari, M. and Taolo, C. (2002). Herd-switching and long-distance dispersal in female African buffalo Syncerus caffer . African Journal of Ecology 40, 97–99.Google Scholar
Hayashida, K., Hara, Y., Abe, T., Yamasaki, C., Toyoda, A., Kosuge, T., Suzuki, Y., Sato, Y., Kawashima, S., Katayama, T., Wakaguri, H., Inoue, N., Homma, K., Tada-Umezaki, M., Yagi, Y., Fujii, Y., Habara, T., Kanehisa, M., Watanabe, H., Ito, K., Gojobori, T., Sugawara, H., Imanishi, T., Weir, W., Gardner, M., Pain, A., Shiels, B., Hattori, M., Nene, V. and Sugimoto, C. (2012). Comparative genome analysis of three eukaryotic parasites with differing abilities to transform leukocytes reveals key mediators of Theileria-induced leukocyte transformation. mBio 3, e00204–e00212.Google Scholar
Horak, I. G., Golezardy, H. and Uys, A. C. (2007). Ticks associated with the three largest wild ruminant species in southern Africa. Onderstepoort Journal of Veterinary Research 74, 231–242.Google Scholar
Jeanmougin, F., Thompson, J. D., Gouy, M., Higgins, D. G. and Gibson, T. J. (1998). Multiple sequence alignment with Clustal X. Trends in Biochemical Sciences 23, 403–405.Google Scholar
Laubscher, L. and Hoffman, L. (2012). An overview of disease-free buffalo breeding projects with reference to the different systems used in South Africa. Sustainability 4, 3124–3140.Google Scholar
Mamabolo, M. V., Ntantiso, L., Latif, A. and Majiwa, P. A. (2009). Natural infection of cattle and tsetse flies in South Africa with two genotypic groups of Trypanosoma congolense . Parasitology 136, 425–431.Google Scholar
Mans, B. J., Pienaar, R., Latif, A. A. and Potgieter, F. T. (2011 a). Diversity in the 18S SSU rRNA V4 hyper-variable region of Theileria in bovines and African buffalo (Syncerus caffer) from southern Africa. Parasitology 138, 766–779.Google Scholar
Mans, B. J., Pienaar, R., Potgieter, F. T. and Latif, A. A. (2011 b). Theileria parva, T. sp. (buffalo) and T. sp. (bougasvlei) 18S variants. Veterinary Parasitology 182, 382–383.Google Scholar
McKeever, D. J. (2009). Bovine immunity – a driver for diversity in Theileria parasites? Trends in Parasitology 25, 269–276.Google Scholar
Muleya, W., Namangala, B., Simuunza, M., Nakao, R., Inoue, N., Kimura, T., Ito, K., Sugimoto, C. and Sawa, H. (2012). Population genetic analysis and sub-structuring of Theileria parva in the northern and eastern parts of Zambia. Parasite and Vectors 5, 255–266.Google Scholar
Oura, C. A., Bishop, R. P., Wampande, E. M., Lubega, G. W. and Tait, A. (2004). Application of a reverse line blot assay to the study of haemoparasites in cattle in Uganda. International Journal for Parasitology 34, 603–613.Google Scholar
Oura, C. A., Asiimwe, B. B., Weir, W., Lubega, G. W. and Tait, A. (2005). Population genetic analysis and sub-structuring of Theileria parva in Uganda. Molecular Biochemistry and Parasitology 140, 229–239.Google Scholar
Oura, C. A., Tait, A., Asiimwe, B., Lubega, G. W. and Weir, W. (2011). Theileria parva genetic diversity and haemoparasite prevalence in cattle and wildlife in and around Lake Mburo National Park in Uganda. Parasitology Research 108, 1365–1374.Google Scholar
Pienaar, R., Potgieter, F. T., Latif, A. A., Thekisoe, O. M. M. and Mans, B. J. (2011 a). Mixed Theileria infections in free-ranging buffalo herds: implications for diagnosing Theileria parva infections in Cape buffalo (Syncerus caffer). Parasitology 138, 884–895.Google Scholar
Pienaar, R., Potgieter, F. T., Latif, A. A., Thekisoe, O. M. M. and Mans, B. J. (2011 b). The HybridII assay: a sensitive and specific real-time hybridization assay for the diagnosis of Theileria parva infection in Cape buffalo (Syncerus caffer) and cattle. Parasitology 138, 884–895.Google Scholar
Puillandre, N., Lambert, A., Brouillet, S. and Achaz, G. (2012). ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Sibeko, K. P., Oosthuizen, M. C., Collins, N. E., Geysen, D., Rambritch, N. E., Latif, A. A., Groeneveld, H. T., Potgieter, F. T. and Coetzer, J. A. W. (2008). Development and evaluation of a real-time polymerase chain reaction test for the detection of Theileria parva infections in Cape buffalo (Syncerus caffer) and cattle. Veterinary Parasitology 155, 37–48.Google Scholar
Spickett, A. M., Horak, I. G., Braack, L. E. and van Ark, H. (1991). Drag-sampling of free-living ixodid ticks in the Kruger National Park. Onderstepoort Journal of Veterinary Research 58, 27–32.Google Scholar
Tamura, K. and Kumar, S. (2002). Evolutionary distance estimation under heterogeneous substitution pattern among lineages. Molecular Biology and Evolution 19, 1727–1736.Google Scholar
Tamura, K. and Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512–526.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.Google Scholar
Zweygarth, E., Koekemoer, O., Josemans, A. I., Rambritch, N., Pienaar, R., Putterill, J., Latif, A. and Potgieter, F. T. (2009). Theileria-infected cell line from an African buffalo (Syncerus caffer). Parasitology Research 105, 579–581.Google Scholar