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Reproduction in Strongyloides (Nematoda): a life between sex and parthenogenesis

Published online by Cambridge University Press:  13 December 2007

A. STREIT
A. STREIT*
Affiliation:
Max Planck Institute for Developmental Biology, Department IV, Evolutionary Biology, Spemannstrasse 37, D-72076 Tübingen, Germany
*
*Corresponding author: Tel: +49 7071 601 403. Fax: +49 7071 601 498. E-mail: [email protected]
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Summary

Nematodes of the genus Strongyloides parasitize the small intestines of vertebrates. In addition to a parasitic life-cycle, which is generally considered to be parthenogenetic, Strongyloides can also have a facultative, free-living generation involving male and female worms. The purpose of the present article was to review the literature on the modes of reproduction, the routes of development in the two generations of Strongyloides, discuss the controversial opinions in the literature regarding these aspects and point to new opportunities for addressing key questions in relation to the biology of reproduction of members of the genus employing genetic and genomic tools.

Keywords

Strongyloidesintestinal nematodesreproductionsex determination
Type
Review Article
Information
Parasitology , Volume 135 , Issue 3 , March 2008 , pp. 285 - 294
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Albertson, D. G., Nwaorgu, O. C. and Sulston, J. E. (1979). Chromatin diminution and a chromosomal mechanism of sexual differentiation in Strongyloides papillosus. Chromosoma 75, 75–87.CrossRefGoogle Scholar
Augustine, D. L. (1940). Experimental studies on the validity of species in the genus Strongyloides. American Journal of Hygiene 32, 24–32.Google Scholar
Basir, M. A. (1950). The morphology and development of the sheep nematode, Strongyloides papillosus (Wedl, 1856). Canadian Journal of Research [D] 28, 173–196.CrossRefGoogle Scholar
Beach, T. D. (1936). Experimental studies on human and primate species of Strongyloides – V. The free-living phase of the life cycle. American Journal of Hygiene 23, 243–277.Google Scholar
Beg, M. K. (1968). Studies on the life-cycle of Strongyloides fulleborni von Linstow, 1905. Annals of Tropical Medicine and Parasitology 62, 502–505.CrossRefGoogle Scholar
Blaxter, M. L., de Ley, P., Garey, J. R., Liu, L. X., Scheldman, P., Vierstraete, A., vanFleteren, J. R., Mackey, L. Y., Dorris, M., Frisse, L. M., Vida, J. T. and Thomas, W. K. (1998). A molecular evolutionary framework for the phylum Nematoda. Nature, London 392, 71–75.CrossRefGoogle ScholarPubMed
Boag, P. R., Newton, S. E. and Gasser, R. B. (2001). Molecular aspects of sexual development and reproduction in nematodes and schistosomes. Advances in Parasitology 50, 153–198.CrossRefGoogle ScholarPubMed
Bolla, R. I. and Roberts, L. S. (1968). Gametogenesis and chromosomal complement in Strongyloides ratti (Nematoda: Rhabdiasoidea). Journal of Parasitology 54, 849–855.CrossRefGoogle ScholarPubMed
Brumpt, E. (1921). Recherches sur le déterminisme des sexes et de l‘évolution des Anguillules parasites (Strongyloides). Comptes rendu hebdomadaires des séances et mémoires de la Société de Biologie et de ses filiales 85, 149–152.Google Scholar
Castagnone-Sereno, P. (2006). Genetic variability and adaptive evolution in parthenogenetic root-knot nematodes. Heredity 96, 282–289.CrossRefGoogle ScholarPubMed
Chang, C. H. and Graham, G. L. (1957). Parasitism, parthenogenesis and polyploidy: the life cycle of Strongyloides papillosus. Journal of Parasitology 43, 13.Google Scholar
Chitwood, B. G. and Graham, G. L. (1940). Absence of vitelline membranes on developing eggs in parasitic females of Strongyloides ratti. Journal of Parasitology 26, 183–190.CrossRefGoogle Scholar
Crook, M. and Viney, M. E. (2005). The effect of non-immune stresses on the development of Strongyloides ratti. Parasitology 131, 383–392.CrossRefGoogle ScholarPubMed
Crook, M., Thompson, F. J., Grant, W. N. and Viney, M. E. (2005). daf-7 and the development of Strongyloides ratti and Parastrongyloides trichosuri. Molecular and Biochemical Parasitology 139, 213–223.CrossRefGoogle ScholarPubMed
Dorris, M., Viney, M. E. and Blaxter, M. L. (2002). Molecular phylogenetic analysis of the genus Strongyloides and related nematodes. International Journal for Parasitology 32, 1507.CrossRefGoogle ScholarPubMed
Eberhardt, A. G., Mayer, W. E. and Streit, A. (2007). The free-living generation of the nematode Strongyloides papillosus undergoes sexual reproduction. International Journal for Parasitology 37, 989–1000. doi: 10.1016/j.ijpara.2007.01.010.CrossRefGoogle ScholarPubMed
Faust, E. C. (1933). Experimantal studies on human and primate species of Strongyloides. II. The development of Strongyloides in the experimental host. American Journal of Hygiene 18, 114–132.Google Scholar
Fisher, M. C. and Viney, M. E. (1998). The population genetic structure of the facultatively sexual parasitic nematode Strongyloides ratti in wild rats. Proceedings of the Royal Society of London, B 265, 703–709.CrossRefGoogle ScholarPubMed
Gemmill, A. W., Viney, M. E. and Read, A. F. (1997). Host immune status determines sexuality in a parasitic nematode. Evolution; International Journal of Organic Evolution 51, 393–401.CrossRefGoogle Scholar
Graham, G. L. (1936). Studies on Strongyloides. I. S. ratti in parasitic series, each generation in the rat established with a single homogonic larva. American Journal of Hygiene 24, 71–87.Google Scholar
Graham, G. L. (1938). Studies on Strongyloides. II. Homogonic and heterogonic progeny of the single homogonically derived S. ratti parasite. American Journal of Hygiene 27, 221–234.Google Scholar
Graham, G. L. (1939 a). Studies on Strongyloides. IV. Seasonal variation in the production of heterogonic progeny by singly established S. ratti from a homogonically derived line. American Journal of Hygiene 30, 15–27.Google Scholar
Graham, G. L. (1939 b). Studies on Strongyloides. V. Constitutional differences between a homogonic and a heterogonic line of S. ratti. Journal of Parasitology 25, 365–375.CrossRefGoogle Scholar
Graham, G. L. (1940). Studies on Strongyloides. VI. Comparison of two homogonic lines of singly established S. ratti. Journal of Parasitology 26, 207–218.CrossRefGoogle Scholar
Grant, W. N., Skinner, S. J., Howes, J. N., Grant, K., Shuttleworth, G., Heath, D. D. and Shoemaker, C. B. (2006 a). Heritable transgenesis of Parastrongyloides trichosuri: a nematode parasite of mammals. International Journal for Parasitology 36, 475–483.CrossRefGoogle ScholarPubMed
Grant, W. N., Stasiuk, S., Newton-Howes, J., Ralston, M., Bisset, S. A., Heath, D. D. and Shoemaker, C. B. (2006 b). Parastrongyloides trichosuri, a nematode parasite of mammals that is uniquely suited to genetic analysis. International Journal for Parasitology 36, 453–466.CrossRefGoogle ScholarPubMed
Grove, D. I. (1989). Historical introduction. In Strongyloidiasis: a Major Roundworm Infection (ed. Grove, D. I.), pp. 1–9. Taylor and Francis, London.Google Scholar
Guiliano, D. B. and Blaxter, M. L. (2006). Operon conservation and the evolution of trans-splicing in the phylum Nematoda. PLoS Genetics 2, e198.CrossRefGoogle ScholarPubMed
Hammond, M. P. and Robinson, R. D. (1994). Chromosome complement, gametogenesis, and development of Strongyloides stercoralis. Journal of Parasitology 80, 689–695.CrossRefGoogle ScholarPubMed
Hannack, E., Kirkham, M., Hymann, A. A. and Oegema, K. (2001). Aurora-A kinase is required for centrosome maturation in Caenorhabditis elegans. Journal of Cell Biology 155, 1109–1116.CrossRefGoogle Scholar
Hansen, E. L., Buecher, E. J. and Cryan, W. S. (1969). Strongyloides fulleborni: environmental factors and free-living generations. Experimental Parasitology 26, 336–343.CrossRefGoogle ScholarPubMed
Harvey, S. C. and Viney, M. E. (2001). Sex determination in the parasitic nematode Strongyloides ratti. Genetics 158, 1527–1533.CrossRefGoogle ScholarPubMed
Harvey, S. C., Gemmill, A. W., Read, A. F. and Viney, M. E. (2000). The control of morph development in the parasitic nematode Strongyloides ratti. Proceedings of the Royal Society of London, B 26, 2057–2063.CrossRefGoogle Scholar
Herrmann, M., Mayer, W. E. and Sommer, R. J. (2006 a). Nematodes of the genus Pristionchus are closely associated with scarab beetles and the Colorado potato beetle in Western Europe. Zoology (Jena) 109, 96–108. doi: 10.1016/j.zool.2006.03.001.CrossRefGoogle ScholarPubMed
Herrmann, M., Mayer, W. E. and Sommer, R. J. (2006 b). Sex, bugs and Haldane's rule: the nematode genus Pristionchus in the United States. Frontiers in Zoology 3, 14. doi: 10.1186/1742-9994-3-14.CrossRefGoogle ScholarPubMed
Hodgkin, J. (2002). Exploring the envelope. Systematic alteration in the sex-determination system of the nematode Caenorhabditis elegans. Genetics 162, 767–780.CrossRefGoogle ScholarPubMed
Junio, A. B., Li, X., Massey, H. C. Jr., Nolan, T. J., Todd Lamitina, S., Sundaram, M. V. and Lok, J. B. (2007). Strongyloides stercoralis: cell- and tissue-specific transgene expression and co-transformation with vector constructs incorporating a common multifunctional 3′ UTR. Experimental Parasitology (in the Press). doi: 10.1016/j.exppora.2007.08.018Google ScholarPubMed
Keiser, P. B. and Nutman, T. B. (2004). Strongyloides stercoralis in the immunocompromised population. Clinical Microbiology Reviews 17, 208–217.CrossRefGoogle ScholarPubMed
Kiontke, K., Gavin, N. P., Raynes, Y., Roehrig, C., Piano, F. and Fitch, D. H. (2004). Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proceedings of the National Academy of Sciences, USA 101, 9003–9008.CrossRefGoogle ScholarPubMed
Kreis, H. A. (1932). Studies on the genus Strongyloides (nematodes). American Journal of Hygiene 16, 450–491.Google Scholar
Li, X., Massey, H. C. Jr., Nolan, T. J., Schad, G. A., Kraus, K., Sundaram, M. and Lok, J. B. (2006). Successful transgenesis of the parasitic nematode Strongyloides stercoralis requires endogenous non-coding control elements. International Journal for Parasitology 36, 671–679.CrossRefGoogle ScholarPubMed
Little, M. D. (1962). Experimental studies on the life cycle of Strongyloides. Journal of Parasitology 48, 41.Google Scholar
Lok, J.B. (2007). Strongyloides stercoralis: a model for translational research on parasitic nematode biology (February 17, 2007). In WormBook ( ed. The C. elegans Research Community). WormBook. doi: 10.1895/wormbook.1.134.1, http://www.wormbook.org.Google Scholar
Massey, H. C., Castelletto, M. L., Bhopale, V. M., Schad, G. A. and Lok, J. B. (2005). Sst-tgh-1 from Strongyloides stercoralis encodes a proposed ortholog of daf-7 in Caenorhabditis elegans. Molecular and Biochemical Parasitology 142, 116–120.CrossRefGoogle ScholarPubMed
Massey, H. C. Jr., Bhopale, M. K., Li, X., Castelletto, M. and Lok, J. B. (2006). The fork head transcription factor FKTF-1b from Strongyloides stercoralis restores DAF-16 developmental function to mutant Caenorhabditis elegans. International Journal for Parasitology 36, 347–352.CrossRefGoogle ScholarPubMed
Matoff, K. (1936). Beobachtungen über die larvale Entwicklung von Strongyloides papillosus (Wedl, 1856) und Infektionsversuche mit filariformen Larven. Parasitology Research 8, 474–491.Google Scholar
Mayer, W. E., Herrmann, M. and Sommer, R. J. (2007). Phylogeny of the nematode genus Pristionchus and implications for biodiversity, biogeography and the evolution of hermaphroditism. BMC Evolutionary Biology 7, 104. doi: 10.1186/1471-2148-7-104.CrossRefGoogle ScholarPubMed
Moncol, D. J. and Triantaphyllou, A. C. (1978). Stronglyoides ransomi: factors influencing the in vitro development of the free-living generation. Journal of Parasitology 64, 220–225.CrossRefGoogle ScholarPubMed
Nigon, V. and Roman, E. (1952). Le déterminisme du sexe et le development cyclique de Strongyloides ratti. Bulletin biologique de la France et de la Belgique 86, 404–448.Google Scholar
Nolan, T. J., Brenes, M., Ashton, F. T., Zhu, X., Forbes, W. M., Boston, R. and Schad, G. A. (2004). The amphidial neuron pair ALD controls the temperature-sensitive choice of alternative developmental pathways in the parasitic nematode, Strongyloides stercoralis. Parasitology 129, 753–759.CrossRefGoogle ScholarPubMed
Nwaorgu, O. C. (1983). The development of the free-living stages of Strongyloides papillosus. I. Effect of temperature on the development of the heterogonic and homogonic nematodes in faecal culture. Veterinary Parasitology 13, 213–223.CrossRefGoogle ScholarPubMed
Pires-daSilva, A. (2007). Evolution of the control of sexual identity in nematodes. Seminars in Cell and Developmental Biology 18, 362–370.CrossRefGoogle ScholarPubMed
Premvati, (1958 a). Studies on Strongyloides of Primates I. Morphology and life history of Strongyloides fuelleborni von Listow, 1905. Canadian Journal of Zoology 36, 65–77.CrossRefGoogle Scholar
Premvati, (1958 b). Studies on Strongyloides of Primates III. Observations on the free-living generations of S. fuelleborni. Canadian Journal of Zoology 36, 447–452.CrossRefGoogle Scholar
Sandground, J. H. (1926). Biological studies on the life-cycle in the genus Strongyloides Grassi, 1879. American Journal of Hygiene 6, 337–388.Google Scholar
Schad, G. A. (1989). Morphology and life history of Strongyloides stercoralis. In Strongyloidiasis: a Major Roundworm Infection of Man (ed. Grove, D. I.), pp. 85–104. Taylor and Francis, London.Google Scholar
Speare, R. (1989). Identification of species of Strongyloides. In Strongyloidiasis: a Major Roundworm Infection of Man (ed. Grove, D. I.), pp. 11–83. Taylor and Francis, London.Google Scholar
Thompson, F. J., Barker, G. L., Hughes, L., Wilkes, C. P., Coghill, J. and Viney, M. E. (2006). A microarray analysis of gene expression in the free-living stages of the parasitic nematode Strongyloides ratti. BMC Genomics 7, 157.CrossRefGoogle ScholarPubMed
Triantaphyllou, A. C. and Moncol, D. J. (1977). Cytology, reproduction, and sex determination of Strongyloides ransomi and S. papillosus. Journal of Parasitology 63, 961–973.CrossRefGoogle ScholarPubMed
Viney, M. E. (1994). A genetic analysis of reproduction in Strongyloides ratti. Parasitology 109, 511–515.CrossRefGoogle ScholarPubMed
Viney, M. E. (1996). Developmental switching in the parasitic nematode Strongyloides ratti. Proceedings of the Royal Society of London, B 263, 201–208.Google ScholarPubMed
Viney, M. E. (1999). Exploiting the life cycle of Strongyloides ratti. Parasitology Today 15, 231–235.CrossRefGoogle Scholar
Viney, M. E. (2002). Environmental control of nematode life cycles. In The Behavioural Ecology of Parasites (ed. Lewis, E. E., Campbell, J. F. and Sukhedo, M. V. K.), pp. 111–128. CAB International, Oxford.CrossRefGoogle Scholar
Viney, M. E. (2006). The biology and genomics of Strongyloides. Medical Microbiology and Immunology 195, 49–54.CrossRefGoogle ScholarPubMed
Viney, M. E. and Lok, J. B. (2007). Strongyloides spp. (May 23, 2007), In WormBook ( ed. The C. elegans Research Community). WormBook, doi: 10.1895/wormbook.1.141.1, http://www.wormbook.org.Google Scholar
Viney, M. E., Matthews, B. E. and Walliker, D. (1992). On the biological and biochemical nature of cloned populations of Strongyloides ratti. Journal of Helminthology 66, 45–52.CrossRefGoogle ScholarPubMed
Viney, M. E., Matthews, B. E. and Walliker, D. (1993). Mating in the nematode parasite Strongyloides ratti: proof of genetic exchange. Proceedings of the Royal Society of London, B 254, 213–219.Google ScholarPubMed
Viney, M. E., Thompson, F. J. and Crook, M. (2005). TGF-beta and the evolution of nematode parasitism. International Journal for Parasitology 35, 1473–1475.CrossRefGoogle ScholarPubMed
Wedl, C. (1856). Über einige Nematoden. Sitzungsberichte der kaiserliche Akademie der Wissenschaften, Wien, Mathematisch-naturwissenschaftliche Classe 19, 122–134.Google Scholar
Wicks, S. R., Yeh, R. T., Gish, W. R., Waterston, R. H. and Plasterk, R. H. (2001). Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nature Genetics 28, 160–164.CrossRefGoogle ScholarPubMed
Yamada, M., Matsuda, S., Nakazawa, M. and Arizono, N. (1991). Species-specific differences in heterogonic development of serially transferred free-living generations of Strongyloides planiceps and Strongyloides stercoralis. Journal of Parasitology 77, 592–594.CrossRefGoogle ScholarPubMed
Zaffagnini, F. (1973). Parthenogenesis in the parasitic and free-living forms of Strongyloides papillosus (Nematoda, Rhabdiasoidea). Chromosoma 40, 443–450.CrossRefGoogle ScholarPubMed