Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-20T00:36:21.997Z Has data issue: false hasContentIssue false
  • English
  • Français

Origins and organization of genetic diversity in natural populations of Trypanosoma brucei

Published online by Cambridge University Press:  06 April 2009

R. E. Cibulskis
R. E. Cibulskis
Affiliation:
Department of Medical Protozoology, London School of Hygiene and Tropical Medicine, Keppel Street, Gower Street, London WC1 7HT
Get access Rights & Permissions [Opens in a new window]

Summary

Experimental work has established that a sexual process can occur in African trypanosomes (Jenni, Marti, Schweizer, Betschart, Le Page, Wells, Tait, Paindavoine, Pays & Steinert, 1986; Paindavoine, Zampetti-Bosseler, Pays, Schweizer, Guyaux, Jenni & Steinert, 1986; Tait, personal communication). However, the role of the process in natural populations of trypanosomes is poorly understood. This paper considers what information can be gained from analyses of isoenzyme polymorphism. A cladistic approach is used to help determine whether trypanosome diversity could have been produced by mutation alone. When applied to three East African populations of Trypanosoma brucei it provides evidence that some diversity has arisen through a sexual process; this explains the variation observed within a locality and can account for the evolution of differences between localities. However, the extent to which genetic exchange currently operates is less clear. Analysis of genotype frequencies indicates that agreements with Hardy-Weinberg expectations can be obtained even if genetic exchange exerted no influence over genotype frequencies. Moreover, analysis of joint locus frequencies reveals disequilibrium between loci and that trypanosome populations may be lacking several genotype combinations. Thus, genetic exchange may not occur sufficiently frequently, or in such a way as to break up associations between loci. The relevance of these observations to the evolution of strain differences within T. brucei is discussed.

Type
Research Article
Information
Parasitology , Volume 96 , Issue 2 , April 1988 , pp. 303 - 322
Copyright
Copyright © Cambridge University Press 1988

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

Beranek, A. P. & Berry, R. J. (1974). Inherited changes in enzyme patterns within parthenogenetic clones of Aphis fabae. Journal of Entomology 48, 141–7.Google Scholar
Brown, A. H. D. (1975). Sample sizes required to detect linkage disequilibrium between two or three loci. Theoretical Population Biology 8, 184–201.Google Scholar
Caugant, D. M., Levin, B. R. & Selander, R. K. (1981). Genetic diversity and temporal variation in the E. coli population of a human host. Genetics 98, 467–90.Google Scholar
Cibulskis, R. E. (1987). Mutation and recombination in the Trypanosomatidae. Annales de Parasitologie Humaine et comparée (in the Press).Google Scholar
Elston, R. C. & Forthofer, R. (1977). Testing for Hardy-Weinberg equilibrium in small samples. Biometrics 33, 536–42.Google Scholar
Emigh, T. H. (1980). A comparison of tests for Hardy-Weinberg equilibrium. Biometrics 36, 627–12.CrossRefGoogle ScholarPubMed
Falrburn, D. J. & Roff, D. A. (1980). Testing genetic models of isoenzyme variability without breeding data: Can we depend on the X 2? Canadian Journal of Fisheries and Aquatic Science 37, 1149–59.Google Scholar
Farris, J. S. (1970). Methods for computing Wagner Trees. Systematic Zoology 19, 83–92.Google Scholar
Farris, J. S. (1972). Estimating phylogenetic trees from distance matrices. American Naturalist 106, 645–68.CrossRefGoogle Scholar
Fitch, W. M. (1977). On the problem of finding the most parsimonious tree. American Naturalist 111, 223–57.Google Scholar
Gibson, W. C. & Borst, P. (1985). Size-fractionation of the small chromosomes of Trypanozoon and Nannomonas trypanosomes by pulsed field gradient gel electrophoresis. Molecular and Biochemical Parasitology 18, 127–10.CrossRefGoogle Scholar
Gibson, W. C., Borst, P. & Fase-Fowler, F. (1985). Further analysis of intraspecific variation in Trypanosoma brucei using restriction site polymorphisms in the maxi-circle of kinetoplast DNA. Molecular and Biochemical Parasitology 15, 21–36.Google Scholar
Gibson, W. C. & Gashumba, J. K. (1983). Isoenzyme characterization of some Trypanozoon stocks from a recent epidemic in Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 114–18.Google Scholar
Gibson, W. C., Marshall, T. F. De C. & Godfrey, D. G. (1980). Numerical analysis of enzyme polymorphism: a new approach to the epidemiology and taxonomy of trypanosomes of the subgenus Trypanozoon. Advances in Parasitology 18, 175–246.CrossRefGoogle Scholar
Gibson, W. C., Osinga, K. A., Michels, P. A. M. & Borst, P. (1985). 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.Google Scholar
Haber, M. (1980). Detection of inbreeding effects by the X 2 test on genotypic and phenotypic frequencies. American Journal of Human Genetics 32, 754–60.Google Scholar
Hebert, P. D. N. (1974 a). Enzyme variability in natural populations of Daphnia magna. II. Genotypic frequencies in permanent populations. Genetics 77, 323–34.Google Scholar
Hebert, P. D. N. (1974 b). Enzyme variability in natural populations of Daphnia magna. III. Genotypic frequencies in intermittent populations. Genetics 77, 335–41.CrossRefGoogle Scholar
Hebert, P. D. N. & Crease, T. (1983). Clonal diversity in populations of Daphnia pulex reproducing by obligate parthenogenesis. Heredity 51, 353–69.CrossRefGoogle Scholar
Hedrick, P., Jain, S. & Holden, L. (1978). Multilocus systems in evolution. Evolutionary Biology 11, 101–84.Google Scholar
Hoffman, R. J. (1986). Variation in contributions of asexual reproduction to the genetic structure of populations of the sea anemone Metridium senile. Evolution 40, 357–65.CrossRefGoogle Scholar
Jaenike, J., Parker, E. D. & Selander, R. K. (1980). Clonal niche structure in the parthenogenetic earthworm Octolasion tyrtaeum. American Naturalist 116, 196–205.CrossRefGoogle Scholar
Jaenike, J. & Selander, R. K. (1979). Evolution and ecology of parthenogenesis in earthworms. American Zoologist 19, 729–37.Google Scholar
Jenni, L., Marti, 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, 173–5.CrossRefGoogle ScholarPubMed
Kimura, M. & Crow, J. F. (1964). The number of alleles that can be maintained in a finite population. Genetics 49, 725–38.CrossRefGoogle Scholar
Kluge, A. G. & Farris, J. S. (1974). Quantitative phyletics and the evolution of anurans. Systematic Zoology 18, 1–32.CrossRefGoogle Scholar
Kunz, B. A. & Haynes, R. H. (1981). Phenomenology and genetic control of mitotic recombination in yeast. Annual Review of Genetics 15, 57–89.CrossRefGoogle ScholarPubMed
Langley, C. H., Smith, D. B. & Johnson, F. M. (1978). Analysis of linkage disequilibrium between allozyme loci in natural populations of Drosophila melanogaster. Genetical Research 32, 215–29.CrossRefGoogle Scholar
Letch, C. A. (1984). A mixed population of Trypanozoon in Glossina palpalis palpalis from Ivory Coast. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 627–30.CrossRefGoogle ScholarPubMed
Levene, H. (1949). On a matching problem arising in genetics. Annals of Mathematical Statistics 20, 91–4.Google Scholar
Levin, B. R. (1981). Periodic selection, infectious gene exchange and the genetic structure of E. coli populations. Genetics 99, 1–23.Google Scholar
Lewontin, R. C. & Cockerham, C. C. (1959). The goodness-of-fit test for detecting natural selection in random mating populations. Evolution 13, 561–4.Google Scholar
Lewontin, R. C. & Felsenstein, J. (1965). The robustness of homogeneity tests in 2 × N tables. Biometrics 21, 19–33.CrossRefGoogle Scholar
Li, C. C. (1955). Population Genetics. Chicago: University of Chicago Press.Google Scholar
Lokki, J. (1976). Genetic polymorphism and evolution in parthenogenetic animals. VII. The amount of heterozygosity in diploid populations. Hereditas 83, 57–64.CrossRefGoogle ScholarPubMed
Lokki, J., Suara, A., Lankinen, P. & Suomalainen, E. (1976 a). Genetic polymorphism and evolution in parthenogenetic animals. V. Triploid Adoxus obscurus (Coleoptera: Chrysomelidae). Genetical Research 28, 27–36.Google Scholar
Lokki, J., Suara, A., Lankinen, P. & Suomalainen, E. (1976 b). Genetic polymorphism and evolution in parthenogenetic animals. VI. Diploid and triploid Polyhydrosus mollis (Coleoptera: Curculionidae). Hereditas 82, 209–16.CrossRefGoogle ScholarPubMed
Lokki, J., Suomalainen, E., Suara, A. & Lankinen, P. (1975). Genetic polymorphism and evolution in parthenogenetic animals. II. Diploid and polyploid Solenobia triquetella (Lepidoptera: Psychidae). Genetics 79, 513–25.Google Scholar
Maynard Smith, J. & Haigh, J. (1974). The hitch-hiking effect of a favourable gene. Genetical Research 23, 23–35.CrossRefGoogle Scholar
Mehlitz, D., Zillman, U. & Sachs, R. (1985). The domestic pig as a carrier of Trypanosoma brucei gambiense in West Africa. Tropenmedizin und Parasitologie 36, Suppl. II. 18.Google Scholar
Mehlitz, D., Zillman, U., Scott, C. M. & Godfrey, D. G. (1982). Epidemiological studies on the animal reservoir of Gambiense sleeping sickness. III. Characterization of Trypanozoon stocks by isoenzymes and sensitivity to human serum. Tropenmedizin und Parasitologie 29, 113–18.Google Scholar
Nei, M. (1975). Molecular Population Genetics and Evolution. Amsterdam: North Holland Publishing Company.Google ScholarPubMed
Ochman, H., Stille, B., Niklasson, M., Selander, R. K. & Templeton, A. R. (1980). Evolution of clonal diversity in the parthenogenetic fly Lonchoptera dubia. Evolution 34, 539–47.CrossRefGoogle ScholarPubMed
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 Tryanosoma brucei stocks and subspecies. Parasitology 92, 31–50.Google Scholar
Paindavoine, P., Zampetti-Bosseler, F., Pays, E., Schweizer, J., Guyaux, M., Jenni, L. & Stetnert, M. (1986). Trypanosome hybrids generated in tsetse flies by nuclear fusion. EMBO Journal 5, 3631–6.CrossRefGoogle ScholarPubMed
Pays, E., Guyaux, M., Aerts, D., Van Meirvenne, N. & Steinert, M. (1985). Reciprocal recombination as a possible mechanism for antigenic variation in trypanosomes. Nature, London 316, 562–4.Google Scholar
Scott, C. M. (1981). Mixed populations of Trypanosoma brucei in a naturally infected pig. Tropenmedizin und Parasitologie 29, 221–2.Google Scholar
Shick, J. M. & Lamb, A. N. (1977). Asexual reproduction and genetic population structure in the colonizing sea anemone Haliplanella luciae. Biological Bulletin 153, 604–17.Google Scholar
Sneath, P. H. A. & Sokal, R. R. (1973). Numerical Taxonomy. San Francisco: W. H. Freeman & Co.Google Scholar
Sokal, R. R. & Rohlf, F. J. (1981). Biometry. San Francisco: W. H. Freeman & Co.Google Scholar
Suara, A., Lokki, J., Lankinen, P. & Suomalatnen, E. (1976). Genetic polymorphism and evolution in parthenogenetic animals. V. Tetraploid Otiorrhynchus scaber (Coleoptera: Curculionidae). Hereditas 82, 79–99.CrossRefGoogle 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, 29–57.Google Scholar
Tait, A. (1985). Genetics of protein variation in populations of parasitic protozoa. In Ecology and Genetics of Host-Parasite Interactions (ed. Anderson, R. M. and Rollinson, D.), pp. 185–203. London: Academic Press.Google Scholar
Tait, A., Barry, J. D., Wink, R., Sanderson, A. & Crowe, J. S. (1985). Enzyme variation in T. brucei ssp. II. Evidence for T. b. rhodesiense being a set of variants of T. b. brucei. Parasitology 90, 89–100.CrossRefGoogle Scholar
Tibayrenc, M., Cariou, M. L. & Solignac, M. (1981). Interpretation génétique des zymogrammes de flagelles des genres Leishmania et Trypanosoma. Comptes rendus, Académie des sciences, Paris 292, 623–5.Google Scholar
Wallace, B. (1958). The comparison of observed and calculated zygotic distributions. Evolution 12, 113–15.CrossRefGoogle Scholar
Ward, R. H. & Sing, C. F. (1970). A consideration of the power of the test to detect inbreeding effects in natural populations. American Naturalist 104, 355–65.Google Scholar
Workman, P. L. (1969). The analysis of simple genetic polymorphisms. Human Biology 41, 97–114.Google Scholar
Young, J. P. W. (1979 a). Enzyme polymorphism and cyclic parthenogenesis in Daphnia magna. I. Selection and clonal diversity. Genetics 92, 953–70.Google Scholar
Young, J. P. W. (1979 b). Enzyme polymorphism and cyclic parthenogenesis in Daphnia magna. II. Heterosis following sexual reproduction. Genetics 92, 971–82.Google Scholar
Zouros, E., Golding, G. B. & MacKay, T. F. C. (1977). The effect of combining alleles into electrophoretic classes on detecting linkage disequilibrium. Genetics 85, 543–50.CrossRefGoogle ScholarPubMed