Hostname: page-component-76fb5796d-vvkck Total loading time: 0 Render date: 2024-04-25T13:13:46.296Z Has data issue: false hasContentIssue false
  • English
  • Français

Parastrongyloides trichosuri suggests that XX/XO sex determination is ancestral in Strongyloididae (Nematoda)

Published online by Cambridge University Press:  19 August 2013

ARPITA KULKARNI ,
ANNA DYKA ,
LINDA NEMETSCHKE ,
WARWICK N. GRANT  and
ADRIAN STREIT
ARPITA KULKARNI
Affiliation:
Department of Evolutionary Biology, Max Planck Institute for Developmental Biology, D-72076 Tübingen, Germany
ANNA DYKA
Affiliation:
Department of Evolutionary Biology, Max Planck Institute for Developmental Biology, D-72076 Tübingen, Germany
LINDA NEMETSCHKE
Affiliation:
Department of Evolutionary Biology, Max Planck Institute for Developmental Biology, D-72076 Tübingen, Germany
WARWICK N. GRANT
Affiliation:
Department of Genetics, La Trobe University, Victoria 3086, Australia
ADRIAN STREIT*
Affiliation:
Department of Evolutionary Biology, Max Planck Institute for Developmental Biology, D-72076 Tübingen, Germany
*
*Corresponding author: Department IV, Max-Planck-Institut für Entwicklungsbiologie, Spemannstrasse 35, D-72076 Tübingen, Germany. E-mail: adrian.streit@tuebingen.mpg.de
Get access Rights & Permissions [Opens in a new window]

Summary

The parasitic roundworms Strongyloides stercoralis (in man) and Strongyloides ratti (in rats) employ environmentally controlled XX/XO sex determination with a pair of X chromosomes and two pairs of autosomes. Strongyloides papillosus (in sheep) has only two pairs of chromosomes, one of which combines the genetic material homologous to the S. ratti chromosomes X and I. This species creates males through the elimination of one copy of the portion related to the X chromosome (chromatin diminution). It is not clear which one of these two sex-determining mechanisms is ancestral. We demonstrate that Strongyloides vituli (in cattle) has two pairs of chromosomes like its very close relative S. papillosus whereas Parastrongyloides trichosuri, a closely related out-group to Strongyloides spp. in Australian brushtail possums, has three chromosome pairs and employs XX/XO sex determination. The X chromosome of P. trichosuri is homologous to the X chromosome of S. ratti. Our data strongly suggest that the last common ancestor of Strongyloides spp. and Parastrongyloides spp. had two pairs of autosomes along with two or one X chromosome in females and males, respectively. The situation with two pairs of chromosomes is likely derived and occurred through the fusion of the X chromosome with an autosome.

Keywords

Parastrongyloides spp.Strongyloides spp.sex determinationX chromosomeevolution
Type
Research Article
Information
Parasitology , Volume 140 , Issue 14 , December 2013 , pp. 1822 - 1830
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

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(Sect. D), 24–32.Google Scholar
Brumpt, E. (1921). Recherches sur le déterminisme des sexes et de l`évolution des Anguillules parasites (Strongyloides). Comptes rendu hebdomadaires des séances et memoires de la Société de Biologie et ses filiales 85, 149–152.Google Scholar
Cowan, P. E., Ralston, M. J., Heath, D. D. and Grant, W. N. (2006). Infection of naive, free-living brushtail possums (Trichosurus vulpecula) with the nematode parasite Parastrongyloides trichosuri and its subsequent spread. International Journal for Parasitology 36, 287–293.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.CrossRefGoogle ScholarPubMed
Eberhardt, A. G., Mayer, W. E., Bonfoh, B. and Streit, A. (2008). The Strongyloides (Nematoda) of sheep and the predominant Strongyloides of cattle form at least two different, genetically isolated populations. Veterinary Parasitology 157, 89–99. doi: 10.1016/j.vetpar.2008.07.019.CrossRefGoogle ScholarPubMed
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
Hammond, M. P. and Robinson, R. D. (1994). Chromosome complement, gametogenesis, and development of Strongyloides stercoralis. Journal of Parasitology 80, 689–695.CrossRefGoogle ScholarPubMed
Harvey, S. C. and Viney, M. E. (2001). Sex determination in the parasitic nematode Strongyloides ratti. Genetics 158, 1527–1533.CrossRefGoogle ScholarPubMed
Mackerras, M. J. (1959). Strongyloides and Parastrongyloides (Nematoda: Rhabdiasoidea) in Australian marsupials. Australian Journal of Zoology 7, 87–104.CrossRefGoogle Scholar
Nemetschke, L., Eberhardt, A. G., Hertzberg, H. and Streit, A. (2010 a). Genetics, chromatin diminution, and sex chromosome evolution in the parasitic nematode genus Strongyloides. Current Biology 20, 1687–1696.CrossRefGoogle ScholarPubMed
Nemetschke, L., Eberhardt, A. G., Viney, M. E. and Streit, A. (2010 b). A genetic map of the animal–parasitic nematode Strongyloides ratti. Molecular and Biochemical Parasitology 169, 124–127.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
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 & Francis, London, UK.Google Scholar
Shao, H., Li, X., Nolan, T. J., Massey, H. C. Jr., Pearce, E. J. and Lok, J. B. (2012). Transposon-mediated chromosomal integration of transgenes in the parasitic nematode Strongyloides ratti and establishment of stable transgenic lines. PLoS Pathogens 8, e1002871. doi: 10.1371/journal.ppat.1002871.CrossRefGoogle ScholarPubMed
Speare, R. (1989). Identification of species of Strongyloides. In Strongyloidiasis: A Major Roundworm Infection of Man (ed. Grove, D. I.), pp. 11–83. Taylor & Francis, London, UK.Google Scholar
Stiernagle, T. (1999). Maintenance of C. elegans. In C. elegans: A Practical Approach (ed. Hope, I. A.), pp. 51–67. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Streit, A. (2008). Reproduction in Strongyloides (Nematoda): a life between sex and parthenogenesis. Parasitology 135, 285–294.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. and Lok, J. B. (2007). Strongyloides spp. (May 23, 2007). In WormBook. doi: 10.1895/wormbook.1.141.1; http://www.wormbook.orgGoogle 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., Green, L. D., Brooks, J. A. and Grant, W. N. (2002). Chemical mutagenesis of the parasitic nematode Strongyloides ratti to isolate ivermectin resistant mutants. International Journal for Parasitology 32, 1677–1682.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
Supplementary material: File

Kulkarni Supplementary Material

Supplementary Material

Download Kulkarni Supplementary Material(File)
File 46.1 KB
Supplementary material: File

Kulkarni Supplementary Material

Table

Download Kulkarni Supplementary Material(File)
File 37.4 KB
Supplementary material: File

Kulkarni Supplementary Material

Table

Download Kulkarni Supplementary Material(File)
File 95.2 KB