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Bank voles (Myodes glareolus) and house mice (Mus musculus musculus; M. m. domesticus) in Europe are each parasitized by their own distinct species of Aspiculuris (Nematoda, Oxyurida)

Published online by Cambridge University Press:  25 August 2015

J. M. BEHNKE ,
A. STEWART ,
A. BAJER ,
M. GRZYBEK ,
P. D. HARRIS ,
A. LOWE ,
A. RIBAS ,
L. SMALES  and
K. J. VANDEGRIFT
J. M. BEHNKE*
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
A. STEWART
Affiliation:
Sir Martin Evans Building, School of Bioscience, Cardiff University, Cardiff CF10 3AX, UK
A. BAJER
Affiliation:
Department of Parasitology, Institute of Zoology, Faculty of Biology, University of Warsaw, 1 Miecznikowa Street, 02-096, Warsaw, Poland
M. GRZYBEK
Affiliation:
Department of Parasitology and Invasive Disease, Faculty of Veterinary Medicine, University of Life Sciences in Lublin, 12 Akademicka Street, 20-950 Lublin, Poland
P. D. HARRIS
Affiliation:
Natural History Museum, University of Oslo, P.O. Box 1172, Oslo N-0316, Norway
A. LOWE
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
A. RIBAS
Affiliation:
Laboratory of Parasitology, Faculty of Pharmacy, University of Barcelona, Avda Diagonal s/n, 08028 Barcelona, Spain
L. SMALES
Affiliation:
Parasitology Section, South Australian Museum, North Terrace, Adelaide 5000, Australia
K. J. VANDEGRIFT
Affiliation:
Center for Infectious Disease Dynamics, The Pennsylvania State University, University Park, PA 16801, USA
*
* Corresponding author. School of Life Sciences, University of Nottingham, University Park Campus, Nottingham NG7 2RD, UK. E-mail: [email protected]
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Summary

The molecular phylogeny and morphology of the oxyuroid nematode genus Aspiculuris from voles and house mice has been examined. Worms collected from Myodes glareolus in Poland, Eire and the UK are identified as Aspiculuris tianjinensis, previously known only from China, while worms from Mus musculus from a range of locations in Europe and from laboratory mice, all conformed to the description of Aspiculuris tetraptera. Worms from voles and house mice are not closely related and are not derived from each other, with A. tianjinensis being most closely related to Aspiculuris dinniki from snow voles and to an isolate from Microtus longicaudus in the Nearctic. Both A. tianjinensis and A. tetraptera appear to represent recent radiations within their host groups; in voles, this radiation cannot be more than 2 million years old, while in commensal house mice it is likely to be less than 10 000 years old. The potential of Aspiculuris spp. as markers of host evolution is highlighted.

Keywords

Myodes glareolusClethrionomys glareolusChionomys nivalisAspiculurisMus musculus musculusMus musculus domesticusbank voleshouse mice
Type
Research Article
Information
Parasitology , Volume 142 , Issue 12 , October 2015 , pp. 1493 - 1505
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Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Adamson, M. L. (1989). Evolutionary biology of the Oxyurida (Nematoda: biofacies of a haplodiploid taxon. Advances in Parasitology 28, 175–228.Google Scholar
Adamson, M. L. (1994). Evolutionary patterns in the life histories of the Oxyurida. International Journal of Parasitology 24, 1167–1177.Google Scholar
Akhtar, S. A. (1955). On nematode parasites of rats and mice of Lahore, with some remarks on the genus Aspiculuris Schulz 1924 and two new species of the genus. Pakistan Journal of Science Research 7, 104–111.Google Scholar
Baird, S. J. E., Ribas, A., Macholan, M., Albrecht, T., Pialek, J. and Gouy de Bellocq, J. (2012). Where are the wormy mice? A re-examination of the hybrid parasitism in the European house mouse hybrid zone. Evolution 66, 2757–2772.Google Scholar
Behnke, J. M. (1974). The Biology of Aspiculuris tetraptera Schultz (Nematoda, Oxyuridae) . Ph.D. thesis. University of London.Google Scholar
Behnke, J. M. (1975). Aspiculuris tetraptera in wild Mus musculus. The prevalence of infection in male and female mice. Journal of Helminthology 49, 85–90.Google Scholar
Behnke, J. M. and Harris, P. D. (2010). Heligmosomoides bakeri – a new name for an old worm? Trends in Parasitology 26, 524–529.Google Scholar
Behnke, J. M., Barnard, C., Hurst, J. L., McGregor, P. K., Gilbert, F. and Lewis, J. W. (1993). The prevalence and intensity of infection with helminth parasites in Mus spretus from the Setubal Peninsula of Portugal. Journal of Helminthology 67, 115–122.Google Scholar
Behnke, J. M., Barnard, C. J., Bajer, A., Bray, D., Dinmore, J., Frake, K., Osmond, J., Race, T. and Sinski, E. (2001). Variation in the helminth community structure in bank voles (Clethrionomys glareolus) from three comparable localities in the Mazury Lake District region of Poland. Parasitology 123, 401–414.Google Scholar
Behnke, J. M., Harris, P. D., Bajer, A., Barnard, C. J., Sherif, N., Cliffe, L., Hurst, J., Lamb, M., Rhodes, A., James, M., Clifford, S., Gilbert, F. S. and Zalat, S. (2004). Variation in the helminth community structure in spiny mice (Acomys dimidiatus) from four montane wadis in the St. Katherine region of the Sinai Peninsula in Egypt. Parasitology 129, 379–398.Google Scholar
Behnke, J. M., Bajer, A., Harris, P. D., Newington, L., Pidgeon, E., Rowlands, G., Sheriff, C., Kuliś-Malkowska, K., Siński, E., Gilbert, F. S. and Barnard, C. J. (2008). Temporal and between-site variation in helminth communities of bank voles (Myodes glareolus) from NE Poland. 2. The infracommunity level. Parasitology 135, 999–1018.CrossRefGoogle ScholarPubMed
Bernard, J. (1987). Parasitic nematode fauna of mammals in Tunisia and neighbouring countries. Les Archives de l'Institut Pasteur Tunis 64, 265–319.Google Scholar
Bjelic-Cabrilo, O., Kostic, D., Popovic, E., Cirkovic, M., Aleksic, N. and Lujic, J. (2011). Helminth fauna of the bank vole Myodes glareolus (Rodentia, Arvicolinae) on the territory of Fruska Gora Mountain (Serbia) – a potential sources of zoonoses. Bulgarian Journal of Agricultural Science 17, 829–836.Google Scholar
Bujalska, G. and Hansson, L. (ed.) (2000). Bank vole biology: recent advances in the population biology of a model species. Polish Journal of Ecology 48 (Suppl.), 1–235.Google Scholar
Carleton, M. D., Musser, G. G. and Pavlinov, I. A. (2003). Myodes Pallas, 1811, is the valid name for the genus of red-backed voles. In Systematics, Phylogeny and Paleontology of Small Mammals. Proceedings of the International Conference devoted to the 90th anniversary of Prof. I.M. Gromov, November 2003, Saint Petersburg (ed. Averianov, A. and Abramson, N.), pp. 96.Google Scholar
Carleton, M. D., Gardner, A. L., Pavlinov, I. Y. and Musser, G. G. (2014). The valid generic name for red-backed voles (Muroidea: Cricetidae: Arvicolinae): restatement of the case for Myodes Pallas, 1811. Journal of Mammology 95, 943–959.Google Scholar
Chaline, J., Brunet-Lecomte, P., Montuire, S., Viriot, L. and Courant, F. (1999). Anatomy of the arvicoline radiation (Rodentia): palaeogeographical, palaeoecological and evolutionary data. Annales Zoologica Fennici 36, 239–267.Google Scholar
Cook, J. A., Runck, A. M. and Conroy, C. J. (2004). Historical biogeography at the crossroads of the northern continents: molecular phylogenetics of red-backed voles (Rodentia: Arvicolinae). Molecular Phylogenetics and Evolution 30, 767–777.CrossRefGoogle ScholarPubMed
Coyne, J. A. and Orr, H. A. (2004). Speciation. Sinauer, Sunderland, Massachusetts.Google Scholar
De Bellocq, J. G., Sara, M., Casanova, S. M., Feliu, C. and Morand, S. (2003). A comparison of the structure of helminth communities in the woodmouse, Apodemus sylvaticus, on islands of the western Mediterranean and continental Europe. Parasitology Research 90, 64–70.Google Scholar
De Bellocq, J. G., Ribas, A., Baird, S. J. E. (2012). New insights into parasitism in the house mouse hybrid zone. Evolution of the House Mouse Series: Cambridge Studies in Morphology and Molecules: New Paradigms in Evolutionary Biology (No. 3). (UK). Cambridge University Press, UK. ISBN 13:9780521760669 Google Scholar
Diesing, K. M. (1861). Revision der Nematoden. Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften. Mathematische/Naturwissenschaftliche Classe 42, 595–736.Google Scholar
Doran, D. J. (1955). A catalogue of the protozoa and helminths of North American Rodents. III. Nematoda. American Midland Naturalist 53, 162–175.Google 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 (Paris) 47, 365–382.Google Scholar
Erickson, A. B. (1938). Parasites of some Minnesota Cricetidae and Zapodidae, and a host catalogue of helminth parasites of native American mice. American Midland Naturalist 20, 575–589.CrossRefGoogle Scholar
Falcón-Ordaz, J., Pulido-Flores, G. and Monks, S. (2010). New species of Aspiculuris (Nematoda: Heteroxynematidae), parasite of Mus musculus (Rodentia: Muridae), from Hidalgo, Mexico. Revista Mexicana de Biodiversidad 81, 669–676.CrossRefGoogle Scholar
Flowerdew, J. R., Gurnell, J. and Gipps, J. H. W. (ed.) (1985). The Ecology of Woodland Rodents. Bank Voles and Wood Mice. The Zoological Society of London, Clarendon Press, Oxford.Google Scholar
Flynn, R. J. (1973). Parasites of Laboratory Animals. Iowa State University Press, Ames.Google Scholar
Fontanilla, I. K. C. and Wade, C. M. (2008). The small subunit (SSU) ribosomal (r)RNA gene as a genetic marker for identifying infective 3rd stage juvenile stage Angiostrongylus cantonensis . Veterinary Parasitology 105, 181–186.Google Scholar
Fuentes, M. V., Cerezuela, A. M. and Galan-Puchades, M. T. (2000). A helminthological survey of small mammals (Insectivores and Rodents) in the Serra Calderona Mountains (Valencian Community, Spain). Research and Reviews in Parasitology 60, 25–35.Google Scholar
Hugot, J. P. (1980). Sur le genre Aspiculuris Schulz. 1924 (Nematoda. Heteroxynematidae). Oxyures parasites de rongeurs Muroidea. Bulletin du Museum National d'Histoire Naturelle. Paris 4 Series 2, 723–735.Google Scholar
Hugot, J. P. (1988). Les Nématodes Syphaciinae, parasites de Rongeurs et de Lagomorphes. Mémoires du Muséum National D'Histoire Naturelle, Série A Zoologie 141, 1–148.Google Scholar
Hugot, J. P. (1999). Primates and their pinworm parasites: the Cameron hypothesis revisited. Systematic Biology 48, 523–546.Google Scholar
Inglis, W. G., Harris, E. A. and Lewis, J. W. (1990). A new species of the nematode genus Aspiculuris Schulz, 1924 from Aethomys namaquensis (Mammalia: Rodentia) in the Kruger National Park, South Africa. Systematic Parasitology 17, 231–236.Google Scholar
Jaarola, M., Martínková, N., Gündüz, I., Brunhoff, C., Zima, J., Nadachowski, A., Amori, G., Bulatova, N. S., Chondropoulos, B., Fraguedakis-Tsolis, S., González-Esteban, J., José López-Fuster, M., Kandaurov, A. S., Kefelioğlu, H., da Luz Mathias, M., Villate, I. and Searle, J. B. (2004). Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 33, 647–663.Google Scholar
Kataranovski, D. S., Vukićević-Radić, O. D., Kataranovski, M. V., Radović, D. L. and Mirkov, I. I. (2008). Helminth fauna of Mus musculus Linnaeus, 1758 from the suburban area of Belgrade, Serbia. Archives of the Biological Society of Belgrade 60, 609–617.Google Scholar
Kinsella, J. M. (1967). Helminths of microtines in western Montana. Canadian Journal of Zoology 43, 269–274.Google Scholar
Kohli, B. A., Speer, K. A., Kilpatrick, C. W., Batsaikhan, N., Damdinbaza, D. and Cook, J. A. (2014). Multilocus systematics and non-punctuated evolution of Holarctic Myodini (Rodentia, Arvicolinae). Molecular Phylogenetics and Evolution 76, 18–29.Google Scholar
Lewis, J. W. (1987). Helminth parasites of British rodents and insectivores. Mammal Review 17, 81–93.Google Scholar
Liu, B., Bu, Y. and Zhang, L. (2012). A new species of Aspiculuris Schulz, 1924 (Nematoda, Heteroxynematidae) from the gray-sided vole, Clethrionomys rufocanus (Rodentia, Cricetidae), from Tianjin, China. Acta Parasitologica 57, 311–315.CrossRefGoogle Scholar
Lou, Y., Zhang, Y., Qiu, J.-H., Gao, J.-F., Wang, W.-T., Xiao, J.-Y., Chang, Q.-C. and Wang, C.-R. (2015). Sequence variability in four mitochondrial genes among pinworm Aspicularis tetraptera isolates from laboratory mice in four provinces, China. Mitochondrial DNA 26, 431–434.Google Scholar
Milazzo, C., Cagnin, M., di Bella, C., Geraci, F. and Ribas, A. (2010). Helminth fauna of commensal rodents, Mus musculus (Linnaeus, 1758) and Rattus rattus (Linnaeus, 1758) (Rodentia, Muridae) in Sicily (Italy). Revista Ibero-Latinoamericana de Parasitologia 69, 194–198.Google Scholar
Miller, M. A., Pfeiffer, W. and Schwartz, T. (2010). Creating the CIPRES Science Gateway for Inference of Large Phylogenetic Trees, pp. 1–8. Gateway Computing Environments Workshop (GCE), New Orleans, LA.Google Scholar
Moulia, C., Aussel, J. P., Bonhomme, F., Boursot, P., Nielsen, J. T. and Renaud, F. (1991). Wormy mice in a hybrid zone: a genetic control of susceptibility to parasite infection. Journal of Evolutionary Biology 4, 679–687.Google Scholar
Musser, G. G. and Carleton, M. D. (2005). Super family Muroidea. In Mammal Species of the World (ed. Wilson, D. E. and Reeder, D. M.), pp. 894–1522. Johns Hopkins University Press, Baltimore.Google Scholar
Nieberding, C., Morand, S., Libois, R. and Michaux, J. R. (2006). Parasites and the island syndrome: the colonization of the western Mediterranean islands by Heligmosomoides polygyrus (Dujardin, 1845). Journal of Biogeography 33, 1212–1222.Google Scholar
Nitzsch, C. L. (1821). Ascaris . In Allgemeine Encyclopadie der Wissenschaften und Kunste (Ersch und Gruber), Leipzig, 6, 44–49.Google Scholar
Okamoto, M., Urushima, H., Iwasa, M. and Hasegawa, H. (2007). Phylogenetic relationships of rodent pinworms (genus Syphacia) in Japan inferred from mitochondrial CO1 gene sequences. Journal of Veterinary Medical Science 69, 545–547.CrossRefGoogle ScholarPubMed
Parel, J. D., Galula, J. U. and Ooi, H. K. (2008). Characterization of rDNA sequences from Syphacia obvelata, Syphacia muris, and Aspiculuris tetraptera and development of a PCR-based method for identification. Veterinary Parasitology 153, 379–383.Google Scholar
Pisanu, B., Chapius, J.-L. and Périn, R. (2003). Syphacia obvelata infections and reproduction of male domestic mice Mus musculus domesticus on a sub-Antarctic Island. Journal of Helminthology 77, 247–253.Google Scholar
Quentin, J. C. (1966). Oxyures des Muridae africains. Annales de Parasitologie Humaine et Comparee 41, 443–452.Google Scholar
Quentin, J. C. (1975). Essai de classification des oxyures Heteroxynematidae. Memoires du Museum National d’ Histoire Naturelle 94, 51–96.Google Scholar
Rishikov, K. M. (1979). [Keys to Helminths of rodents in the USSR. Nematodes and Acanthocephala] (In Russian), pp. 272. AN SSSR, Moscow.Google Scholar
Ryan, S. and Holland, C. (1996). The intestinal helminth community of wild woodmice Apodemus sylvaticus in County Wicklow. Biology and environment. Proceedings of the Royal Irish Academy 96B, 45–48.Google Scholar
Sage, R. D., Heyneman, D., Kee-Chong, L. and Wilson, A. C. (1986). Wormy mice in a hybrid zone. Nature 324, 60–63.Google Scholar
Sainz-Elipe, S., Galan-Puchades, M. T. and Fuentes, M. V. (2007). The helminth community of the Mediterranean mouse, Mus spretus, in a post-fire regenerated Mediterranean ecosystem. Helminthologia 44, 107–111.Google Scholar
Schmalz, E. (1831). XIX Tabulae Anatomium Entozoorum. Illustrantes. Dresden and Leipzig, Libraria Arnoldi.Google Scholar
Schulz, R. Ed. (1927). On the genus Aspiculuris Schulz, 1924, and two new species of it – A. dinniki and A. asiatica, from rodents. Annals of Tropical Medicine and Parasitology 21, 267–275.Google Scholar
Schulz, R. E. S. (1924). Oxuyridae of Armenian mice. Trudy Tropiceskogo Instituta Armenii (Reports of the Tropica Institute of Armenia) 2, 41–51.Google Scholar
Sharpe, G. I. (1964). The helminth parasites of some small mammal communities. I. The parasites and their hosts. Parasitology 54, 145–154.Google Scholar
Singleton, G. R., Brown, P. R., Pech, R. P., Jacob, J., Mutze, G. J. and Krebs, C. J. (2005). One hundred years of eruptions of house mice in Australia – a natural biological curio. Biological Journal of the Linnean Society 84, 617–627.Google Scholar
Skirnisson, K., Eydal, M., Gunnarsson, E. and Hersteinsson, P. (1993). Parasites of the arctic fox (Alopex lagopus) in Iceland. Journal of Wildlife Diseases 29, 440–446.CrossRefGoogle ScholarPubMed
Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014, 1–2.Google Scholar
Suzuki, H., Nunome, M., Kinoshita, G., Aplin, K. P., Vogel, P., Kryukov, A. P., Jin, M-L., Han, S-H., Maryanto, I., Tsuchiya, K., Ikeda, H., Shiroishi, T., Yonekawa, H. and Moriwaki, K. (2013). Evolutionary and dispersal history of Eurasian house mice Mus musculus clarified by more extensive geographic sampling of mitochondrial DNA. Heredity 111, 375–390.Google Scholar
Taffs, L. F. (1976). Pinworm infections in laboratory rodents: a review. Laboratory Animals 10, 1–13.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Tattersall, F. H., Nowell, F. and Smith, R. H. (1994). A review of the endoparasites of wild house mice Mus domesticus . Mammal Review 24, 61–71.Google Scholar
Tesakov, A. S., Lebedev, V. S., Bannikova, A. A. and Abramson, N. I. (2010). Clethrionomys Tilesius, 1850 is the valid generic name for red-backed voles and Myodes Pallas, 1811 is a junior synonym of Lemmus Link, 1795. Russian Journal of Theriology 9, 83–86.Google Scholar
Thomas, R. J. (1953). On the nematodes and trematode parasites of some small mammals from the Inner Hebrides. Journal of Helminthology 28, 143–168.Google Scholar