Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-26T21:29:18.591Z Has data issue: false hasContentIssue false

Genetic exchange and evolutionary relationships in protozoan and helminth parasites

Published online by Cambridge University Press:  06 April 2009

A. Tait
Affiliation:
Wellcome Unit of Molecular Parasitology, University of Glasgow, Glasgow G61 1QH

Summary

The study of genetic exchange systems and the use of genetic analysis has been relatively limited in parasites leading to considerable gaps in our basic knowledge. This lack of knowledge makes it difficult to draw firm conclusions as to how these systems evolved. An additional problem is also raised by the difficulties in defining evolutionary distances particularly with the unicellular protozoa, using classical ultrastructural and cytological criteria. While these difficulties have by no means been overcome, the use of rapid sequencing techniques applied to the ribosomal genes has allowed measurement of evolutionary distances, and considerable advances in our understanding of the genetic exchange systems in a few parasitic protozoa have recently been made. The conclusions from these recent sets of analyses are reviewed and then examined together in order to discuss the evolution of genetic exchange systems in parasitic protozoa. The evolutionary distances defined by ribosome sequence analysis show that parasites are an extremely divergent group, with distances which, in some cases, are orders of magnitude greater than the distances between mammals and fish; furthermore these studies suggest that the parasitic protozoa or their free-living ancestors are extremely ancient. These findings support the view that parasitism has occurred independently many times and that the parasitic life-style has been adopted by evolutionarily distinct groups. The recent observation of a non-obligatory genetic exchange system in the diploid but evolutionarily ancient kinetoplastid Trypanosoma brucei suggests that diploidy and meiosis are extremely old. The observation, in parasitic protozoa and helminths, that selfing or non-obligatory mating is a common feature suggests that these processes may be strategies to overcome the cost of meiosis. In this context, the question of what selective forces maintain genetic exchange is discussed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

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

Baker, J. R. (1989). Sexual processes in parasitic protozoa. International Journal for Parasitology 19, 465–72.CrossRefGoogle ScholarPubMed
Ball, S. J., Pitillo, R. M. & Long, P. M. (1989). Intestinal and extraintestinal life cycle of emeriid coccidia. Advances in Parasitology 29, 154.Google Scholar
Baroin, A., Perasso, R., Qu, L.-H., Brugerolle, G., Backellerie, J.-P. & Adoutte, A. (1988). Partial phylogeny of unicellular eukaryotes based on rapid sequencing of a portion of 285 ribosomal RNA. Proceedings of the National Academy of Sciences, USA 85, 3474–8.CrossRefGoogle Scholar
Borst, P., Ploeg, van der M., Hoek, van J. F. M., Tas, J. & James, J. (1982). On the DNA content and ploidy of trypanosomes. Molecular and Biochemical Parasitology 6, 1323.CrossRefGoogle ScholarPubMed
Brenner, S. (1974). The genetics of Caenorhabdisis elegans. Genetics 77, 7194.CrossRefGoogle ScholarPubMed
Elwood, H. J., Olsen, G. J. & Sogin, M. L. (1985). The small subunit ribosomal RNA gene sequences from the hyportichous ciliates Oxytricha nova and Stlonychia pustula. Journal of Molecular Evolution 2, 399410.Google Scholar
Erdman, V. A. & Walters, J. (1986). Collection of published 5S, 5·8S and 4·5S ribosomal RNA sequences. Nucleic Acid Research 14, r1–r59.CrossRefGoogle Scholar
Evans, D. A., Kennedy, W. P., Elbihari, S., Chapman, C. J., Smith, V. & Peters, W. (1987). Hybrid formation within the genus Leishmania? Parasitology 29, 165–73.Google ScholarPubMed
Fenton, B. & Walliker, D. (1990). Genetic analysis of polymorphic proteins of the human malaria parasite Plasmodium falciparum. Genetic Research (in the press).CrossRefGoogle ScholarPubMed
Fenton, B., Walker, A. & Wallirer, D. (1985). Protein variation in clones of Plasmodium falciparum detected by two dimensional electrophoresis. Molecular and Biochemical Parasitology 16, 173–83.CrossRefGoogle ScholarPubMed
Gibson, W. C. (1989). Analysis of a genetic cross between T. brucei rhodesiense and T.b. brucei. Parasitology 99, 391401.CrossRefGoogle ScholarPubMed
Gibson, W. C., Osinga, K. A., Michaels, P. A. M. & Borst, P. (1985). Trypanosomes of the subgenus Trypanozoon are diploid for housekeeping genes. Molecular and Biochemical Parasitology 16, 231–42.CrossRefGoogle ScholarPubMed
Glassberg, J., Miyazaki, L. & Rifkin, M. R. (1985). Isolation and partial characterisation of mutants of the trypanosomatid Crithidia fasciculata and their use in detecting genetic recombination. Journal of Protozoology 32, 118–25.CrossRefGoogle ScholarPubMed
Gunderson, J. H., McCutchan, T. F. & Sogin, M. L. (1986). Sequence of the small sub-unit RNA gene expressed in the blood stream stages of Plasinodiuin berghei: evolutionary implications. Journal of Protozoology 33, 525–9.CrossRefGoogle Scholar
Hamilton, M. D. (1983). Pathogens as causes of genetic diversity in their host populations. In Population Biology of Infectious Diseases (ed. Anderson, R. M. & May, R. M.), pp. 269296. Berlin: Springer-VerlagGoogle Scholar
Hasegawa, M., Iida, Y., Yano, T., Takqiwa, F. & Iwabuchi, M. (1985). Phylogenetic relationships among eukaryotic kingdoms inferred from ribosomal RNA sequences. Journal of Molecular Evolution 22, 32–8.CrossRefGoogle ScholarPubMed
Hassouna, N., Michot, B. & Bachellerie, J. P. (1984). Improved methods for structure probing in large RNAs: a rapid heterologous sequencing approach is coupled to the direct mapping of nuclease accessible sites. Application to the 5' terminal domain of eukaryotic 28s RNA. Nucleic Acids Research 11, 5903–20.Google Scholar
Hori, H. & Oscwa, S. (1986). Evolutionary change in 5'S r-RNA secondary structure and a phylogenetic tree of 352 5'S r-RNA species. Biosysteins 19, 163–72.CrossRefGoogle Scholar
Jeffers, T. K. (1974). Genetic transfer of anti-coccidial drug resistance in Eimeria tenella. Journal of Parasitology 60, 900–4.CrossRefGoogle Scholar
Jenni, L., Marti, S., Schwelzer, 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, 171–95.CrossRefGoogle ScholarPubMed
Johnson, A. M. & Baverstock, P. R. (1989). Rapid ribosomal RNA sequencing and the phylogenetic analysis of protists. Parasitology Today 5, 102–5.CrossRefGoogle ScholarPubMed
Johnson, A. M., Murray, P. J., Illana, S. & Baverstock, P. J. (1987). Rapid nucleotide sequence analysis of the small sub-unit ribosomal RNA of Toxoplasma gondii: evolutionary implications for the apicomplexa. Molecular and Biochemical Parasitology 25, 239–46.CrossRefGoogle Scholar
Johnson, A. M., Thanon, A., Boreham, P. F. L. & Baverstock, P. R. (1989). Blastocystis homminis: Phvlogenetic affinities determined by r-RNA sequence comparison. Experimental Parasitology 68, 283–8.CrossRefGoogle Scholar
Joyner, L. P. & Norton, C. C. (1977). Further observations on the genetic transfer of drug resistance in Eirneria maxima. Parasitology 74, 205–13.CrossRefGoogle Scholar
Lake, J. A., de la Cruz, V. F., Ferreirra, P. C. G., Morel, C. & Simpson, L. (1988). Evolution of parasitism: kinetoplastid history reconstructed from mitochondrial r-RNA gene sequences. Proceedings of the National Academy of Sciences, USA 85, 4779–83.CrossRefGoogle Scholar
Lane, D. J., Pace, B., Olsen, G. J., Stal, D. A., Sogin, M. L. & Pace, N. R. (1985). Rapid determination of 16s ribosomal RNA sequences for phylogenetic analysis. Proceedings of the National Academy of Sciences, USA 82, 6955–9.CrossRefGoogle Scholar
Page, Le R. W. F., Wells, J. P., Prospero, T. D. & Sternberg, J. (1988). Genetic analysis of hybrid T. brucei. In Current Communications in Molecular Biology: Molecular Genetics of Parasitic Protozoa, (ed. Turner, M. J. & Arnott, D.), pp. 6571. New York: Cold Spring Harbor.Google Scholar
Levine, N. D., Corliss, J. O., Cox, F. E. G., Deroux, G. F., Loeblich, A. R., Lom, J., Lynn, D., Merinfield, E. G., Page, F. C., Poljansky, G., Sprague, V., Vavra, J. & Wallace, F. G. (1980). A newly revised classification of the Protozoa. Journal of Protozoology 27, 3758.CrossRefGoogle ScholarPubMed
Lewis, W. M. (1987). The cost of sex. In The Evolution of Sex and its Consequences (ed. Steans, S. C.), pp. 87105. Basel: Birkhauser.Google Scholar
Smith, Maynard J. (1978). The Evolution of Sex. Cambridge: Cambridge University Press.Google Scholar
Melhorn, H. & Schein, E. (1984). The piroplasms: life cycle and sexual stages. Advances in Parasitology 23, 37103.CrossRefGoogle Scholar
Miles, M. A. (1988). Viruses of parasitic protozoa. Parasitology Today 4, 289–90.CrossRefGoogle ScholarPubMed
McCarroll, R., Olsen, G. H., Stalil, Y. D., Woese, C. R. & Sogin, M. L. (1983). Nucleotide sequence of the Dictiostelium discoideum small sub-unit ribosomal RNA inferred from the gene sequence: evolutionary implications. Biochemistry 22, 5858–68.CrossRefGoogle Scholar
Nanney, D. L. (1980). Experimental Ciliatology. New York: John Wiley & Sons.Google Scholar
Nicholas, W. L. (1984). The Biology of Free-living Nematodes. Oxford: Clarendon Press.Google Scholar
Nollen, P. M. (1983). Patterns of sexual reproduction among parasitic platyhelniinths. Parasitology 86, 99120.CrossRefGoogle Scholar
Paindavoine, P., Zampetti—Bosseler, F., Pays, E., Schweizer, J., Guyaux, M., Jenni, L. & Steinert, M. (1986). Trypanosome hybrids generated in tsetse flies by nuclear fusion. European Molecular Biology Organization Journal 5, 3631–6.CrossRefGoogle ScholarPubMed
Perasso, R., Baroin, A., Qu, L.-M., Bachellerie, J. P. & Adoutte, A. (1989). Origin of the algae. Nature, London 339, 142–4.CrossRefGoogle ScholarPubMed
Pfefferkorn, L. C. & Pfefferkorn, E. R. (1980). Toxoplasma gondii. Genetic recombination between drug resistant mutants. Experimental Parasitology 50, 305–16.CrossRefGoogle ScholarPubMed
Preparata, R. M., Meyer, E. B., Preparata, F. P., Simon, E. M., Vossbrinck, C. R. & Nanney, D. L. (1989). Ciliate evolution: the ribosomal phylogenies of the Tetrahymenine ciliates. Journal of Molecular Evolution 28, 427–41.CrossRefGoogle ScholarPubMed
Qu, L.-H., Hardman, N., Gill, L., Chappell, L. H., Nicoloso, M. & Bachellerie, J.-P. (1986). Phylogeny of helminths determined by r-RNA sequence comparison. Molecular and Biochemical Parasitology 20, 93–9.CrossRefGoogle Scholar
Qu, L.-H., Nicoloso, M. & Bachalleri, J. P. (1988). Phylogenetic callibration of the 5' terminal domain of large r-RNA achieved by determining twenty eukaryotic sequence. Journal of Molecular Evolution 28, 113–24.CrossRefGoogle Scholar
Qu, L.-H., Michot, B. & Bachellerie, J. P. (1983). Improved methods for structure probing in large RNAs: a rapid ‘heterologous’ sequencing approach is coupled to the direct mapping of nuclease accessible sites. Application to the 5' terminal domain of eukaryotic 28 S r-RNA. Nucleic Acids Research 11, 5903–20.CrossRefGoogle Scholar
Rollinson, D., Joyner, L. P. & Norton, C. C. (1979). Eimeria maxima: the use of enzyme markers to detect the genetic transfer of drug resistance between lines. Parasitology 78, 361–7.CrossRefGoogle ScholarPubMed
Rosario, V. E. (1976). Genetics of chloroquine resistance in malaria parasites. Nature, London 261, 585–6.CrossRefGoogle ScholarPubMed
Rudzinska, M. A., Spielman, A., Lewencrub, S., Tracer, W. & Piesman, J. (1983). Sexuality in piroplasms as revealed by electron microscopy in Babesia microti. Proceedings of the National Academy of Sciences, USA 80, 2966–70.CrossRefGoogle ScholarPubMed
Sargeaunt, P. C., Jackson, T. F. H. G., Wiffen, S. R. & Bhojuani, R. (1988). Biological evidence of genetic exchange in Entamoeba histolvtica. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 862–7.CrossRefGoogle Scholar
Schweizer, J., Tait, A. & Jenni, L. (1988). The timing of hybrid formation in African trypanosomes during cyclical transmission. Parasitology Research 75, 98101.CrossRefGoogle ScholarPubMed
Sharkey, A., Langsley, G., Patarapotikul, J., Mercereau-Puijalon, O., Mclean, A. & Walliker, D. (1988). Chromosome size variation in the malaria parasite of rodents Plasmodium chabaudi. Molecular and Biochemical Parasitology 28, 4754.CrossRefGoogle ScholarPubMed
Shirley, M. W. (1978). Electrophoretic variation of enzymes: a further marker for genetic studies of Eimeria. Zeitschrift für Parasitology 57, 83–7.CrossRefGoogle ScholarPubMed
Sinnis, P. & Wellems, P. (1988). Long-range restriction maps of Plasmodium falciparum chromosomes: crossing over and size variation among geographically distant isolates. Genomics 3, 287–95.CrossRefGoogle ScholarPubMed
Sogin, M. L., Elwood, H. J. & Gunderson, J. H. (1986 a). Evolutionary diversity of eukaryotic small-sub Unit r-RNA genes. Proceedings of the National Academy of Sciences, USA 83, 1383–7.CrossRefGoogle Scholar
Sogin, M. L., Gunderson, J. H., Elwood, H. J., Alonso, R. A. & Peattie, D. A. (1989). Phylogenetic meaning of the Kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science 243, 75–7.CrossRefGoogle ScholarPubMed
Sogin, M. L., Swanton, M. T., Gunderson, J. H. & Elwood, H. J. (1986 b). Sequence of the small ribosomal RNA gene from the hypotrichous ciliate Euplotes aediculatus. Journal of Protozoology 33, 26–9.CrossRefGoogle ScholarPubMed
Sternberg, 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 a new hybrid genotype. Molecular and Biochemical Parasitology 27, 191200.CrossRefGoogle ScholarPubMed
Sternberg, J., Turner, C. M. R., Wells, J. M., Ranford-Cartwright, L. C., le Page, R. W. F. & Tait, A. (1989). Gene exchange in African trypanosomes: frequency and allelic segregation. Molecular and Biochemical Parasitology 34, 269–80.CrossRefGoogle ScholarPubMed
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., Turner, C. M. R. & Sternberg, J. (1988). Genetic exchange in Trypanosoma brucei: allelic segregation and reassortment. In Current Communications in Molecular Biology: Molecular Genetics of Parasitic Protozoa (ed. Turner, M. J. & Arnott, D.), pp. 5864. New York: Cold Spring Harbor.Google Scholar
Tait, A., Turner, C. M. R., 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
Tait, A. & Turner, C. M. R. (1990). Genetic exchange in Trypanosoma brucei. Parasitology Today (in the press).CrossRefGoogle ScholarPubMed
Thaitong, S., Beale, G. H., Fenton, B., Mcbride, J. S., Rosario, V. E., Walker, A. & Walliker, D. (1984). Clonal variation in a single isolate of the malaria parasite Plasmodium falciparum. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 242–5.CrossRefGoogle Scholar
Tibayrenc, M., Ward, P., Moya, A. & Ayala, F. J. (1986). National populations of the T. cruzi, the agent of Chagas disease, have a complex multiclonal structure. Proceedings of the National Academy of Sciences, USA 83, 115–19.CrossRefGoogle Scholar
Tibayrenc, M., Echalar, L., Dujardin, J. P., Poch, O. & Desjeux, P. (1984). The microdistribution of isoenzyme strains of Trypanosoma cruzi: in Southern Bolivia: new isoenzyme profiles and further arguments against Mendelian sexuality. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 519–25.CrossRefGoogle ScholarPubMed
Turner, C. M. R., Sternberg, J., Smith, E., Buchanan, N., Hide, G. & Tait, A. (1990). Evidence that the mechanism of gene exchange in Trypanosoma brucei involves meiosis and syngamy. Parasitology (in the press).CrossRefGoogle ScholarPubMed
Walliker, D. (1983). The Contribution of Genetics to the Study of Parasitic Protozoa. Letchworth, U.K. and John Wiley, New York: Research Studies Press.Google Scholar
Walliker, D. (1989). Genetic recombination in malaria parasites. Experimental Parasitology 69, 303–9.CrossRefGoogle ScholarPubMed
Walliker, D., Carter, R. & Morgan, S. (1973). Genetic recombination in Plasmodium berghei. Parasitology 66, 309–20.CrossRefGoogle ScholarPubMed
Walliker, D., Carter, R. & Sanderson, A. (1975). Genetic studies in Plasmodium chabaudi: recombination between enzyme markers. Parasitology 70, 1924.CrossRefGoogle ScholarPubMed
Walliker, D., Quakyl, I. A., Wellems, T. E., McCutchan, T. F., Szarfinan, A., Corcoran, L. M., Burkot, T. R. & Carter, H. (1987). Genetic analysis of the human malaria parasite P. falciparum. Science 236, 1661–6.CrossRefGoogle Scholar
Wellems, T. E., Walliker, D., Smith, S. L., Rosario, V. E., Maloy, W. L., Howard, B. J., Carter, R. & McCutchan, T. F. (1987). A histidine—rich protein gene marks a linkage group favoured strongly in a genetic cross of Plasmodium falciparum. Cell 49, 633–42.CrossRefGoogle Scholar
Wells, J. M., Prospero, T. D., Jenni, L. & le Page, R. W. F. (1987). DNA contents and molecular karyotypes of hybrid Trypanosoma brucei. Molecular and Biochemical Parasitology 24, 103–16.CrossRefGoogle ScholarPubMed
Wilson, A. C., Carlson, S. S. & White, T. J. (1977). Biochemical evolution. Annual Review of Biochemistry 46, 473639.CrossRefGoogle ScholarPubMed
Whitfield, P. J. & Evans, N. A. (1983). Platyhelminth parthenogenesis and amixis. Parasitology 86, 121–60.CrossRefGoogle Scholar
Yang, Y. J., Desser, S. S. & Fallis, A. M. (1971). Elongate and round gametes of Leucocytozoon simondi in ducks innoculated with megaschizonts. Journal of Protozoology 18, 553–6.CrossRefGoogle Scholar
Zhang, Q., Tibayrenc, M. & Ayala, F. J. (1988). Linkage disequilibrium in natural populations of Trypanosoma cruzi (flagellate), the agent of Chagas' Disease. Journal of Protozoology 35, 81–5.CrossRefGoogle ScholarPubMed