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Molecular evidence that Heligmosomoides polygyrus from laboratory mice and wood mice are separate species

Published online by Cambridge University Press:  15 March 2006

J. CABLE
Affiliation:
School of Biosciences, Cardiff University, Cardiff CF10 3TL, UK
P. D. HARRIS
Affiliation:
School of Biology, University of Nottingham, Nottingham NG7 2RD, UK
J. W. LEWIS
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey TW20 OEX, UK
J. M. BEHNKE
Affiliation:
School of Biology, University of Nottingham, Nottingham NG7 2RD, UK

Abstract

The gastro-intestinal (GI) nematode Heligmosomoides polygyrus is an important experimental model in laboratory mice and a well-studied parasite of wood mice in the field. Despite an extensive literature, the taxonomy of this parasite in different hosts is confused, and it is unclear whether laboratory and field systems represent the same or different Operational Taxonomic Units (OTUs). Molecular analyses reveal high sequence divergence between H. p. bakeri (laboratory) and H. p. polygyrus (field); 3% difference in the ribosomal DNA Internal Transcribed Spacers (ITS) and 8·6% variation in the more rapidly evolving mitochondrial cytochrome c oxidase I (COI) gene. The COI sequence of U.K. H. p. polygyrus is more similar to H. glareoli from voles than to H. p. bakeri, while a single isolate of H. p. polygyrus from Guernsey confirms the extent of genetic variation between H. p. polygyrus populations. Analysis of molecular variance demonstrated that mtCOI sequence variation is associated primarily with groups with distinct ITS2 sequences, and with host identity, but is not partitioned significantly with a single combined taxon H. polygyrus incorporating European and North American isolates. We conclude therefore that the laboratory OTU should be raised to the level of a distinct species, as H. bakeri from the laboratory mouse Mus musculus, and we reject the hypothesis that H. bakeri has diverged from H. polygyrus in the recent past following introduction into America. However, we are unable to reject the hypothesis that H. polygyrus and H. bakeri are sister taxa, and it may be that H. polygyrus is polyphyletic or paraphyletic.

Type
Research Article
Copyright
2006 Cambridge University Press

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References

REFERENCES

Abu-Madi, M. A., Behnke, J. M., Lewis, J. W. and Gilbert, F. S. ( 1998). Descriptive epidemiology of Heligmosomoides polygyrus in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology 72, 93100.CrossRefGoogle Scholar
Abu-Madi, M. A., Pleass, R. J. and Lewis, J. W. ( 1994). Metabolic labelling of wild and laboratory subspecies of the trichostrongyle nematode Heligmosomoides polygyrus. Veterinary Parasitology 55, 235243.CrossRefGoogle Scholar
Abu-Madi, M. A., Behnke, J. M., Lewis, J. W. and Gilbert, F. S. ( 2000 a). Seasonal and site specific variation in the component community structure of intestinal helminths in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology 74, 3144.Google Scholar
Abu-Madi, M. A., Mohd-Zain, S. N., Lewis, J. W. and Reid, A. P. ( 2000 b). Genomic variability within laboratory and wild isolates of the trichostrongyle mouse nematode Heligmosomoides polygyrus. Journal of Helminthology 74, 195201.Google Scholar
Adams, B. J. ( 1998). Species concepts and the evolutionary paradigm in modern nematology. Journal of Nematology 30, 121.Google Scholar
Anderson, T. J. C. ( 1995). Ascaris infections in humans from North America: molecular evidence for cross-infection. Parasitology 110, 215219.CrossRefGoogle Scholar
Asakawa, M. ( 1988). Genus Heligmosomoides Hall, 1916 (Heligmosomidae: Nematoda) from the Japanese wood mice, Apodemus spp. II. A review of the genus Heligmosomoides with the establishment of the phylogenetic lines of known species. Journal of the College of Dairying 12, 349365.Google Scholar
Asakawa, M. ( 1991). Genus Heligmosomoides Hall, 1916 (Heligmosomidae: Nematoda) from Japanese Islands. Helminthologia 28, 155163.Google Scholar
Asakawa, M. and Ohbayashi, M. ( 1986). Genus Heligmosmoides Hall, 1916 (Heligmosomidae: Nematoda) from the Japanese wood mice, Apodemus spp. I. A taxonomic study on four taxon of the genus Heligmosomoides from three species of the Japanese Apodemus spp. Journal of the College of Dairying 11, 317331.Google Scholar
Audebert, F., Chilton, N. B., Justine, J., Gallut, C., Tillier, A. and Durette-Desset, M. C. ( 2005). Additional molecular evidence to support a sister taxon relationship between Heligmosomoidea and Molineoidea nematodes (Trichostrongyloidea). Parasitology Research 96, 343346.CrossRefGoogle Scholar
Avise, J. ( 2000). Phylogeography. Harvard University Press, London.
Barnard, C. J., Behnke, J. M., Gage, A. R., Brown, H. and Smithurst, P. R. ( 1998). The role of parasite-induced immunodepression, rank and social environment in the modulation of behaviour and hormone concentration in male laboratory mice (Mus musculus). Proceedings of the Royal Society of London Series B 265, 693701.CrossRefGoogle Scholar
Behnke, J. M. ( 1987). Evasion of immunity by nematode parasites causing chronic infections. Advances in Parasitology 26, 170.CrossRefGoogle Scholar
Behnke, J. M., Keymer, A. E. and Lewis, J. W. ( 1991). Heligmosomoides polygyrus or Nematospiroides dubius? Parasitology Today 7, 177179.Google Scholar
Behnke, J. M., Lewis, J. W., Mohd-Zain, S. N. and Gilbert, F. S. ( 1999). Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections. Journal of Helminthology 73, 3144.Google Scholar
Berry, R. J. ( 1985). Evolutionary and ecological genetics of the bank vole and wood mouse. In The Ecology of Woodland Rodents ( ed. Flowerdew, J. R., Gurnell, J. and Gipps, J. H. W.) Symposium of the Zoological Society of London 55, 132.
Blouin, M. S. ( 2002). Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus Internal Transcribed Spacer. International Journal for Parasitology 32, 527531.CrossRefGoogle Scholar
Blouin, M. S., Yowell, C. A., Courtney, C. H. and Dame, J. B. ( 1997). Haemonchus placei and Haemonchus contortus are separate species based on mtDNA evidence. International Journal for Parasitology 27, 13831387.CrossRefGoogle Scholar
Burg, R. W. and Stapley, E. O. ( 1989). Isolation and characterization of the producing organism. In Ivermectin and Abamectin ( ed. Campbell, W. C.), pp. 2432. Springer-Verlag, New York.CrossRef
Chilton, N. B., Gasser, R. B. and Beveridge, I. ( 1997). Phylogenetic relationships of Australian strongyloid nematodes inferred from ribosomal DNA sequence data. International Journal for Parasitology 27, 14811494.CrossRefGoogle Scholar
Durette-Desset, M. C. ( 1971). Essai de classification des nematodes Heligmosomes. Correlations avec la Paleobiogeographie des hôtes. Memoires du Musée d' Histoire Naturelle 69, 1126.Google Scholar
Durette-Desset, M. C. ( 1985). Trichostrongyloid nematodes and their vertebrate hosts: reconstruction of the phylogeny of a parasitic group. Advances in Parasitology 24, 239303.CrossRefGoogle Scholar
Durette-Desset, M. C., Kinsella, J. M. and Forrester, D. J. ( 1972). Arguments en faveur de la double origine des nematodes nearctiques du genre Heligmosomoides Hall, 1916. Annales de Parasitologie 47, 365382.CrossRefGoogle Scholar
Excoffier, L., Smouse, P. E. and Quattro, J. M. ( 1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479491.Google Scholar
Eyualem, A. and Blaxter, M. ( 2003). Comparison of biological, molecular and morphological methods of species identification in a set of cultured Panagrolaimus isolates. Journal of Nematology 35, 119128.Google Scholar
Folmer, O., Black, M., Hoeth, W., Lutz, R. and Vrijenhoek, R. C. ( 1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit from diverse marine invertebrates. Molecular and Marine Biology and Biotechnology 3, 294299.Google Scholar
Forrester, D. J. and Neilson, J. T. M. ( 1973). Comparative infectivity of Heligmosomoides polygyrus (=Nematospiroides dubius) in three species of Peromyscus. Journal of Parasitology 59, 251255.CrossRefGoogle Scholar
Gasser, R. B., Nansen, P. and Guldberg, P. ( 1996). Fingerprinting sequence variation in ribosomal DNA of parasites by DGGE. Molecular and Cellular Probes 10, 99105.CrossRefGoogle Scholar
Gasser, R. B., Zhu, X., Beveridge, I. and Chilton, N. B. ( 2001). Sequence heterogeneity in the second internal transcribed spacer (rDNA) within some members of the Hypodontus macropi (Nematoda, Strongyloidea) complex. Electrophoresis 22, 10761085.3.0.CO;2-8>CrossRefGoogle Scholar
Genov, T. and Yanchev, Y. ( 1981). Morphology and taxonomy of the nematodes of the genera Heligmosomoides Hall, 1916 and Heligmosomum Railliet et Henry, 1909 (Heligmosomidae Cram, 1927) from Bulgaria. Khelmintologiya 12, 830.Google Scholar
Gregory, R. D., Montgomery, S. S. J. and Montgomery, W. I. ( 1992). Population biology of Heligmosomoides polygyrus (Nematoda) in the wood mouse. Journal of Animal Ecology 61, 749757.CrossRefGoogle Scholar
Hillis, D. M. and Dixon, M. T. ( 1991). Ribosomal DNA: molecular evolution and phylogenetic inference. Quarterly Review of Biology 66, 411453.CrossRefGoogle Scholar
Hoste, H., Gasser, R. B., Chilton, N. B., Mallet, S. and Beveridge, I. ( 1993). Lack of intraspecific variation in the second internal transcribed spacer (ITS-2) of Trichostrongylus colubriformis ribosomal DNA. International Journal for Parasitology 23, 10691071.CrossRefGoogle Scholar
Hugall, A., Stanton, J. and Moritz, C. ( 1999). Reticulate evolution and the origins of ribosomal internal transcribed spacer diversity in apomictic Meloidogyne. Molecular Biology and Evolution 16, 157164.CrossRefGoogle Scholar
Kavaliers, M., Colwell, D. D., Braun, W. J. and Choleris, E. ( 2003). Brief exposure to the odour of a parasitized male alters the subsequent mate odour responses of female mice. Animal Behaviour 65, 5968.CrossRefGoogle Scholar
Keymer, A. E. and Slater, A. F. G. ( 1990). Animal models and epidemiology. In Hookworm Disease: Current Status and New Directions ( ed. Schad, G. and Warren, K. S.), pp. 129144. Taylor and Francis, London.
Mayer, M. S. and Soltis, P. S. ( 1999). Intraspecific phylogeny analysis using ITS sequences: insights from studies of the Streptanthus glandulosus (Cruciferae). Systematic Botany 24, 4761.CrossRefGoogle Scholar
Monroy, F. G. and Enriquez, F. J. ( 1992). Heligmosomoides polygyrus: a model for chronic gastrointestinal helminthiasis. Parasitology Today 8, 4954.CrossRefGoogle Scholar
Nieberding, C., Morand, S., Libois, R. and Michaux, J. R. ( 2004 a). A parasite reveals cryptic phylogeographic history of its host. Proceedings of the Royal Society, Series B 271, 25592568.Google Scholar
Nieberding, C., Libois, R., Douady, C. J., Morand, S. and Michaux, J. R. ( 2004 b). Phylogeography of a nematode (Heligmosomoides polygyrus) in the western Palaearctic region: persistence of northern cryptic populations during ice ages? Molecular Ecology 14, 765779.Google Scholar
Posada, D. and Buckley, T. A. ( 2004). Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology 53, 793808.CrossRefGoogle Scholar
Posada, D. and Crandall, K. A. ( 1998). Modeltest: Testing the model of DNA substitution. Bioinformatics 14, 817818.CrossRefGoogle Scholar
Pritchard, D. I., Lawrence, C. E., Appleby, P., Gibb, I. A. and Glover, K. ( 1994). Immunosuppressive proteins secreted by the gastrointestinal nematode parasite Heligmosomoides polygyrus. International Journal for Parasitology 24, 495500.CrossRefGoogle Scholar
Quinnell, R. J. ( 1992). The population dynamics of Heligmosomoides polygyrus in an enclosure population of wood mice. Journal of Animal Ecology 61, 669679.CrossRefGoogle Scholar
Quinnell, R. J., Behnke, J. M. and Keymer, A. E. ( 1991). Host specificity of and cross-immunity between two strains of Heligmosomoides polygyrus. Parasitology 102, 419427.CrossRefGoogle Scholar
Schneider, S., Roessli, D. and Excoffier, L. ( 2000). Arlequin: a software for population genetics data analysis. Ver 2.000. Genetics and Biometry laboratory, Department of Anthropology, University of Geneva, Switzerland.
Scott, M. E. and Tanguay, G. V. ( 1994). Heligmosomoides polygyrus: a laboratory model for direct life cycle nematodes of humans and livestock. In Parasitic and Infectious Diseases ( ed. Scott, M. E. and Smith, G.), pp. 279300. Academic Press Inc., New York.
Sites, J. W. and Marshall, J. C. ( 2004). Operational criteria for delimiting species. Annual Review of Ecology and Systematics 35, 199227.CrossRefGoogle Scholar
Spurlock, G. M. ( 1943). Observations on host-parasite relations between laboratory mice and Nematospiroides dubius. Journal of Parasitology 29, 303311.CrossRefGoogle Scholar
Sukhdeo, S. C., Sukhdeo, M. V. K., Black, M. B. and Vrijenhoek, R. C. ( 1997). The evolution of tissue migration in parasitic nematodes (Nematoda: Strongylida) inferred from a protein-coding mitochondrial gene. Biological Journal of the Linnaean Society 61, 281298.CrossRefGoogle Scholar
Swofford, D. L. ( 2003). PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.
Tenora, F. and Barus, V. ( 2001). Synonymy of the nematode Heligmosomoides polygyrus (Heligmosomidae) and notes on validity of related species. Helminthologia 38, 176.Google Scholar
Tenora, F., Barus, V. and Prokes, M. ( 2003). Notes to the species Heligmosomoides polygyrus (Dujardin, 1845) (Nematoda, Heligmosomoidae) parasitizing Rodentia. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 51, 718.Google Scholar
Zhu, X. Q., D'Amelio, S., Palm, H. W., Paggi, L., George-Nascimento, M. and Gasser, R. B. ( 2002). SSCP-based identification of members within the Pseudoterranova decipiens complex (Nematoda: Ascaridoidea: Anisakidae) using genetic markers in the internal transcribed spacers of ribosomal DNA. Parasitology 124, 615623.CrossRefGoogle Scholar