Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-23T06:58:10.679Z Has data issue: false hasContentIssue false

Population genetics of Trypanosoma brucei in Central Africa: taxonomic and epidemiological significance

Published online by Cambridge University Press:  06 April 2009

P. Truc
Affiliation:
UMR CNRS/ORSTOM 9926: ‘Génétique moléculaire des parasites et des vecteurs’, ORSTOM, BP 5045, 34032 Montpellier Cédex 01, France
M. Tibayrenc
Affiliation:
UMR CNRS/ORSTOM 9926: ‘Génétique moléculaire des parasites et des vecteurs’, ORSTOM, BP 5045, 34032 Montpellier Cédex 01, France

Summary

In order to estimate the value of population genetics for both the taxonomy of trypanosomes belonging to the species Trypanosoma brucei and a better understanding of Human African Trypanosomiasis (HAT), we undertook a cellulose acetate electrophoresis isoenzyme study involving 55 stocks isolated from man and animals in Congo, Zaire and Cameroun. Out of the 24 loci surveyed, 15 exhibited variability, which made it possible to delimit 23 zymodemes, divided into 2 groups. The first group equated to the classical subspecies Trypanosoma brucei gambiense, while the second corresponded to the classical subspecies Trypanosoma brucei brucei. These results broadly agree with the current taxonomy, and are corroborated by RFLP analysis of kDNA. Statistical analysis indicates a basically clonal reproduction system of the trypanosomes in the area studied; the zymodemes are equivalent to natural clones (or a family of closely related clones), stable in space and time. Epidemiological hypotheses are proposed according to the geographic distribution of the clones in this area.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

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

Aerts, D., Truc, P., Penchenier, L., Claes, Y. & Le Ray, D. (1992). A kit for in vitro isolation of trypanosomes in the field: First trial with sleeping sickness patients in the Congo. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 394–5.CrossRefGoogle ScholarPubMed
Apted, F. I. C. (1970). Clinical manifestations and diagnosis of sleeping sickness. In The African Trypanosomiases (ed. Mulligan, H. W.), pp. 661683. London: George Allen and Unwin.Google Scholar
Bienen, E. J., Hammadi, E. & Hill, G. C. (1980). Initiation of trypanosome transformation from bloodstream trypomastigotes to procyclic trypomastigotes. Journal of Parasitology 66, 680–2.CrossRefGoogle ScholarPubMed
Borst, P. & Fase Fowler, F. (1979). The maxi-circle of Trypanosoma brucei kinetoplast DNA. Biochimica et Biophysica Acta 565, 112.CrossRefGoogle ScholarPubMed
Borst, P., Fase Fowler, F. & Gibson, W. C. (1981). Quantitation of genetic differences between Trypanosoma brucei gambiense, rhodesiense and brucei by restriction enzyme analysis of kinetoplast DNA. Molecular and Biochemical Parasitology 3, 117–31.CrossRefGoogle ScholarPubMed
Borst, P., Fase Fowler, F., Frasch, A. C. C., Hoeijmakers, J. H. J. & Weijers, P. J. (1980 a). Characterization of DNA from Trypanosoma brucei and related trypanosomes by restriction endonuclease digestion. Molecular and Biochemical Parasitology 1, 221–46.Google Scholar
Borst, P., Fase Fowler, F., Hoeijmakers, J. H. J. & Frasch, A. C. C. (1980 b). Variations in maxi-circle and mini-circle sequences in the kinetoplast DNAs from different Trypanosoma brucei strains. Biochimica et Biophysica Acta 610, 197210.CrossRefGoogle ScholarPubMed
Cibulskis, R. E. (1988). Origins and organization of genetic diversity in natural populations of Trypanosoma brucei. Parasitology 96, 303–22.Google ScholarPubMed
Cibulskis, R. E. (1992). Genetic variation in Trypanosoma brucei and the epidemiology of sleeping sickness in the Lambwe Valley, Kenya. Parasitology 104, 99109.CrossRefGoogle ScholarPubMed
Cunningham, I. (1977). New culture medium for maintenance of tsetse tissues and growth of trypanosomatids. Journal of Protozoology 21, 325–9.CrossRefGoogle Scholar
Dukes, P., Kaukas, A., Hudson, K. M., Asonganyi, T. & Gashumba, J. K. (1989). A new method for isolating Trypanosoma brucei gambiense from sleeping sickness patients. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 636–9.CrossRefGoogle ScholarPubMed
Dye, C. (1991). Population genetics of nonclonal, nonrandomly mating malaria parasites. Parasitology Today 7, 236–40.CrossRefGoogle ScholarPubMed
Frezil, J. L. (1983). La Trypanosomiase Humaine en République Populaire du Congo. Travaux et Documents ORSTOM155, Paris.Google Scholar
Gibson, W. C. (1986). Will the real Trypanosoma brucei gambiense please stand up. Parasitology Today 2, 255–7.CrossRefGoogle ScholarPubMed
Gibson, W. C., Borst, P. & Fase Fowler, F. (1985 a). Further analysis of intraspecific variation in Trypanosoma brucei using restriction site polymorphisms in the maxi-circle of kinetoplast DNA. Molecular and Biochemical Parasitology 15, 2136.CrossRefGoogle ScholarPubMed
Gibson, W. C. & Gashumba, J. K. (1983). Isoenzyme characterization of some Trypanozoon stocks from a recent trypanosomiasis epidemic in Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 114–18.CrossRefGoogle ScholarPubMed
Gibson, W. C., Marshall, T. F. & Godfrey, D. G. (1980). Numerical analysis of enzyme polymorphism: a new approach to the epidemiology and taxonomy of trypanosomes of subgenus Trypanozoon. Advances in Parasitology 18, 175246.CrossRefGoogle Scholar
Gibson, W. C., Mehlitz, D., Lanham, S. & Godfrey, D. G. (1978). The identification of Trypanosoma brucei gambiense in Liberian pigs and dogs by isoenzymes and by resistance to human plasma. Tropenmedizin und Parasitologic 29, 335–45.Google ScholarPubMed
Gibson, W. C., Osinga, K. A., Michels, P. A. M. & Borst, P. (1985 b). Trypanosomes of subgenus Trypanozoon are diploid for housekeeping genes. Molecular and Biochemical Parasitology 16, 231–42.CrossRefGoogle ScholarPubMed
Gibson, W. C. & Wellde, B. T. (1985). Characterization of Trypanozoon stocks from the South Nyanza sleeping sickness focus in Western Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 671–6.CrossRefGoogle ScholarPubMed
Godfrey, D. G., Baker, R. D., Rickman, L. R. & Mehlitz, D. (1990). The distribution, relationships and identification of enzymic variants within the subgenus Trypanozoon. Advances in Parasitology 29, 139.CrossRefGoogle ScholarPubMed
Godfrey, D. G. & Kilgour, V. (1976). Enzyme electrophoresis in characterizing the causative organism of Gambian trypanosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 70, 219–24.Google ScholarPubMed
Hide, G., Cattand, P., Le Ray, D., Barry, J. D. & Tait, A.(1990). The identification of Trypanosoma brucei sub-species using repetitive DNA sequences. Molecular and Biochemical Parasitology 39, 213–26.CrossRefGoogle Scholar
Hoare, C. A. (1972). The Trypanosomes of Mammals.A Zoological Monograph. Oxford: Blackwell Scientific Publications.Google Scholar
Jacquard, A. (1973). Distances généalogiques et distances génétiques. Cahiers d' Anthropologic et d' Ecologie humaine 1, 11124.Google Scholar
Jenni, L., Martin, S., Schweizer, J., Betschart, B., Le Page, R. W. F., Wells, J. M., Tait, A., Paindavoine, P., Pays, E. & Steinert, M. (1986). Hybrid formation between African trypanosomes during cyclical transmission. Nature, London 322, 171–5.CrossRefGoogle ScholarPubMed
Kageruka, P., Colaert, I. & Ngimbi, N. P. (1977). Strain of Trypanosoma (Trypanozoon) brucei isolated from pigs in Bas-Zaïre. Annates de la Sociét&eeacute; beige de Médecine Tropicale 57, 85–8.Google ScholarPubMed
Kooy, R. F., Hirumi, H., Moloo, S. K., Nantulya, V. M., Dukes, P., van der Lindin, P. M., Duijndan, W. A. L., Janse, C. J. & Overdulve, J. P. (1989). Evidence for diploidy in metacyclic forms of African trypanosomes. Proceedings of the National Academy of Sciences, USA 86, 5469–72.CrossRefGoogle ScholarPubMed
Magnus, E., Vervoort, T. & van Meirvenne, N. (1978). A card agglutination test with stained trypanosomes (CATT) for the serological diagnosis of Trypanosoma brucei gambiense trypanosomiasis. Annales de la Société belge de Médecine Tropicale 58, 169–76.Google Scholar
Makumyaviri, A., Mehlitz, D., Kageruka, P., Kazyumba, G. L. & Molisho, D. (1989). Le réservoir animal de Trypanosoma brucei gambiense au Zaïre: infections trypanosomiennes dans deux foyers du Bas-Zaïre. Tropenmedizin und Parasitologie 40, 258–62.Google ScholarPubMed
Mathieu-Daudé, F. (1991). Mode de reproduction de Trypanosoma brucei dans ses populations naturelles: implications taxonomiques et épidémiologiques. Thèse ès Sciences, Université Montpellier II.Google Scholar
Mehlitz, D. (1986). Le réservoir animal de la maladie du sommeil à Trypanosoma brucei gambiense. Etudes et synthèses de I'IEMVT. Ed. Deutsche Gesellschaft für Technische Zusammenarbeit (GTZ), Eschborn, RFA 16, 156 pp.Google Scholar
Mehlitz, D., Zillmann, U., Scott, C. M. & Godfrey, D. G. (1982). Epidemiological studies on the animal reservoir of gambiense sleeping sickness. 3: Characterization ofTrypanozoon stocks by isoenzyme and sensitivity to human serum. Tropenmedizin und Parasitologie 33, 113–18.Google Scholar
Mihok, S., Otieno, L. H. & Darji, N. (1990). Population genetics of Trypanosoma brucei and the epidemiology of human sleeping sickness in the Lambwe Valley, Kenya. Parasitology 100, 219–33.CrossRefGoogle ScholarPubMed
Miles, M. & Ward, R. (1978). Preliminary isoenzyme studies on phlebotomine sandflies (Diptera: Psychodidae). Annals of Tropical Medicine and Parasitology 35, 105–8.Google Scholar
Nei, M. (1972). Genetic distances between populations. The American Naturalist 106, 283–92.CrossRefGoogle Scholar
Noireau, F., Gouteux, J. P., Toudic, A., Samba, F. & Frezil, J. L. (1986). Importance épidémiologique duréservoir animal à Trypanosoma brucei gambiense au Congo. 1: Prévalence des trypanosomiases animales dans les foyers de maladie du sommeil. Tropenmedizi und Parasitologie 37, 393–8.Google Scholar
Noireau, F., Paindavoine, P., Lemesre, J. L., Toudic, A., Pays, E., Gouteux, J. P., Steinert, M. & Frezil, J. L. (1989). The epidemiological importance of the animal reservoir of Trypanosoma brucei gambiense in the Congo. II: Characterization of the T. brucei complex. Tropenmedizin und Parasitologie 40, 911.Google Scholar
Paindavoine, P., Pays, E., Laurent, M., Geltmeyer, Y., Le Ray, D., Mehlitz, D. & Steinert, M. (1986). The Use of DNA hybridization and numerical taxonomy in determining relationships between Trypanosoma brucei stocks and sub-species. Parasitology 92, 3150.CrossRefGoogle Scholar
Paindavoine, P., Zampetti-Bosseler, F., Coquelet, H., Pays, E. & Steinert, M. (1989). Different allele frequencies in Trypanosoma brucei brucei and T. b. gambiense populations. Molecular and Biochemical Parasitology 32, 6172.CrossRefGoogle Scholar
Scott, C. M., Frezil, J. L., Toudic, A. & Godfrey, D. G. (1983). The sheep as a potential reservoir of human trypanosomiasis in the Republic of Congo. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 397401.CrossRefGoogle Scholar
Selander, R. K. & Levin, B. R. (1980). Genetic diversity and structure in Escherichia coli populations. Science 210, 245–7.Google ScholarPubMed
Shapiro, S. Z., Naessens, J., Liesangang, B., Moloo, S. K. & Magondu, J. (1984). Analysis by flow cytometry of DNA synthesis during the life-cycle of African trypanosomes. Acta Tropica 41, 312–13.Google ScholarPubMed
Steinberg, J., Tait, A., Haley, S., Wells, J. M., Le Page, R. W. F., Schweizer, J. & Jenni, L. (1988). Genetic exchange in African trypanosomes; characterisation of new hybrid genotype. Molecular and Biochemical Parasitology 27, 191200.CrossRefGoogle Scholar
Stevens, J. R., Lanham, S. M., Allingham, R. & Gashumba, J. K. (1992). A simplified method for identifying subspecies and strain groups in Trypanozoon by isoenzymes. Parasitology (in the Press).Google ScholarPubMed
Stevens, J. R., Nunes, V. L. B., Lanham, S. M. & Oshiro, E. T. (1989). Isoenzyme characterization of Trypanosoma evansi isolated from capybaras and dogs in Brazil. Acta Tropica 46, 213–22.CrossRefGoogle ScholarPubMed
Suomalainen, E., Saura, A. & Lokki, J. (1976). Evolution of parthenogenetic insects. Evolutionary Biology 9, 209–67.Google Scholar
Tait, A. (1980). Evidence for diploidy and mating in Trypanosomes. Nature, London 287, 536–8.CrossRefGoogle ScholarPubMed
Tait, A. (1983). Sexual processes in the kinetoplastida. Parasitology 86, 2957.CrossRefGoogle ScholarPubMed
Tait, A., Babiker, E. A. & Le Ray, D. (1984). Enzyme variation in Trypanosoma brucei ssp. I: Evidence for the sub-speciation of Trypanosoma brucei gambiense. Parasitology 89, 311–26.CrossRefGoogle ScholarPubMed
Tait, A. & Turner, C. M. R. (1990). Genetic exchange in Trypanosoma brucei. Parasitology Today 6, 70–5.CrossRefGoogle ScholarPubMed
Tait, A., Turner, C. M. R. T., Le Page, R. W. F. & Wells, J. M. (1989). Genetic evidence that metacyclic forms of Trypanosoma brucei are diploid. Molecular and Biochemical Parasitology 37, 247–56.CrossRefGoogle ScholarPubMed
Tibayrenc, M. & Ayala, F. J. (1988). Isozyme variability in Trypanosoma cruzi, the agent of Chagas' disease: Genetical, taxonomical and epidemiological significance. Evolution 42, 2, 277–92.Google ScholarPubMed
Tibayrenc, M. & Ayala, F. J. (1991). Towards a population genetics of microorganisms: the clonal theory of parasitic protozoa. Parasitology Today 7, 228–32.CrossRefGoogle ScholarPubMed
Tibayrenc, M., Kjellberg, F. & Ayala, F. J. (1990). A clonal theory of parasitic protozoa: the population structures of Entamoeba, Giardia, Leishmania, Naegleria, Plasmodium, Trichomonas and Trypanosoma and their medical and taxonomical consequences. Proceedings of the National Academy of Sciences, USA 87, 2414–18.CrossRefGoogle ScholarPubMed
Tibayrenc, M., Kjellberg, F, Arnaud, J., Oury, B., Breniere, S. F., Darde, M. L. & Ayala, F. J. (1991). Are eucaryotic microorganisms clonal or sexual? A population genetics vantage. Proceedings of the National Academy of Sciences, USA 88, 5129–33.CrossRefGoogle ScholarPubMed
Tibayrenc, M., Ward, P., Moya, A. & Ayala, F. J. (1986). Natural populations of Trypanosoma cruzi, the agent of Chagas disease, have a multiclonal structure. Proceedings of the National Academy of Sciences, USA 83, 115–19.CrossRefGoogle ScholarPubMed
Truc, P. (1991). Apport de la génétique des populations à la taxonomie de Trypanosoma brucei et à l'épidémiologie de la Trypanosomiase Humaine en Afrique Centrale. Thèse ès Sciences, Université Montpellier II.Google Scholar
Truc, P., Mathieu-Daudé, F. & Tibayrenc, M. (1991). Multilocus isozyme identification of Trypanosoma brucei stocks isolated from Central Africa: evidence for an animal reservoir of sleeping sickness in Congo. Acta Tropica 49, 127–35.CrossRefGoogle ScholarPubMed
Woo, P. T. K. (1970). The haematocrit centrifuge technique for the diagnosis of African trypanosomiasis. Acta Tropica 27, 384–6.Google ScholarPubMed
Zillmann, U., Mehlitz, D. & Sachs, R. (1984). Identity of Trypanozoon stocks and domestic dogs in Liberia. Tropenmedizin und Parasitologie 35, 105–8.Google ScholarPubMed