Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-22T12:18:41.236Z Has data issue: false hasContentIssue false

Sexual transmission of a nematode parasite of Wood Mice (Apodemus sylvaticus)?

Published online by Cambridge University Press:  06 May 2004

J. R. CLARKE
Affiliation:
Department of Zoology, Oxford University, South Parks Road, Oxford OX1 3PS, UK
T. J. C. ANDERSON
Affiliation:
Department of Genetics, Southwest Foundation for Biomedical Research, PO Box 760549, San Antonio, Texas 78345, USA
C. BANDI
Affiliation:
DIPAV, Sezione di Patologia Generale e Parassitologia, Università degli Studi di Milano, Via Celoria 10, 20133, Milano, Italy

Abstract

Sexual transmission occurs commonly in microparasites such as viruses and bacteria, but this is an unusual transmission route for macroparasites. Here we present evidence which suggests that a nematode parasite of Wood Mice (Apodemus sylvaticus) may be sexually transmitted and we have classified the nematode using molecular data. Wood Mice were collected annually in the course of work on their reproductive physiology. Larval nematodes were found in the epididymides of 19·6% of males. It seems likely that they would be transmitted to females at ejaculation. To identify these larval nematodes, which we were unable to do using morphological features, we sequenced the 18S rDNA. Sequence comparisons with the molecular phylogeny of Blaxter et al. (1998) demonstrated that they were bursate nematodes (Order Strongylida). The relationships between strongylid taxa were poorly resolved by 18S rDNA. However, both distance and parsimony analyses grouped the nematode with the superfamily Metastrongylidea in a clade containing Filaroides and Angiostrongylus sp. Importantly, the sequences were distinct from those of Heligmosomoides polygyrus and Angiostrongylus dujardini, two common strongylid nematodes of Apodemus. We were therefore unable positively to identify these worms by matching their sequences with those from morphologically identifiable adult strongylid nematodes infecting Apodemus. These results demonstrate that an as yet unidentified strongylid is quite commonly found in large numbers in the male reproductive tract of Wood Mice. Further work is required to understand the biology and transmission dynamics of this interesting system.

Type
Research Article
Copyright
2004 Cambridge University Press

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

ASKAWA, M. & TENORA, F. (1996). A checklist of epidemiology of nematode parasites of the genus Apodemus (Murinae: Rodentia) throughout the world excluding Japan. Journal of Rakuno Gakuen University 20, 181213.Google Scholar
ATTILI, V. R., HIRA, S. K. & DUBE, M. K. (1983). Schistosomal genital granulomas: a report of 10 cases. British Journal of Venereal Diseases 59, 269272.CrossRefGoogle Scholar
BAKER, J. R. (1930). The breeding seasons in British wild mice. Proceedings of the Zoological Society of London 1930, 113126.CrossRefGoogle Scholar
BLAXTER, M. L., DE LEY, P., GAREY, J. R., LIU, L. X., SCHELDEMAN, P., VIERSTRAETE, A., VANFLETEREN, J. R., MACKEY, L. Y., DORRIS, M., FRISSE, L. M., VIDA, J. T. & THOMAS, W. K. (1998). A molecular evolutionary framework for the phylum Nematoda. Nature, London 392, 7175.CrossRefGoogle Scholar
BROWN, E. D., MACDONALD, D. W., TEW, T. E. & TODD, I. A. (1994 a). Apodemus sylvaticus infected with Heligmosomoides polygyrus (Nematoda) in an arable ecosystem: epidemiology and effects of infection on the movement of male mice. Journal of Zoology, London 234, 623640.Google Scholar
BROWN, E. D., MACDONALD, D. W., TEW, T. E. & TODD, I. A. (1994 b). Rhythmicity of egg production by Heligmosomoides polygyrus in Wood Mice, Apodemus sylvaticus. Journal of Helminthology 68, 105108.Google Scholar
CARRENO, R. A. & NADLER, S. A. (2003). Phylogenetic analysis of the Metastrongyloidea (Nematoda: Strongylida) inferred from ribosomal RNA gene sequences. Journal of Parasitology 89, 965973.CrossRefGoogle Scholar
CHITTY, D. & KEMPSON, D. A. (1949). Prebaiting small mammals and a new design of live trap. Ecology 30, 536542.CrossRefGoogle Scholar
DOUGLAS, J. R. & BAKER, J. M. (1959). The chronology of intrauterine infection with Toxocara canis (Werner 1782) in the dog. Journal of Parasitology 45, 4344.Google Scholar
DROZDZ, J. & DOBY, J. M. (1970). Angiostrongylus dujardini sp.n. (Nematoda: Metastrongyloidea) parasite de Apodemus sylvaticus et Clethrionomys glareolus. Bulletin de la Société Zoologique de France 95, 659.Google Scholar
ELTON, C., FORD, E. B., BAKER, J. R. & GARDNER, A. D. (1931). The health and parasites of a wild mice population. Proceedings of the Zoological Society of London 1931, 657721.Google Scholar
FLOWERDEW, J. R., GURNELL, J. & GIPPS, J. H. W. (1985). The Ecology of Woodland Rodents: Bank Voles and Wood Mice. Symposia of the Zoological Society of London, Number 25. Clarendon Press, Oxford.
FORRESTER, D. J. & SENGER, C. M. (1964). Prenatal infection of bighorn sheep with Protostrongylid lungworms. Nature, London 201, 1051.CrossRefGoogle Scholar
GAILLARD, C. & STRAUSS, F. (1990). Ethanol precipitation of DNA with polyacrylamide as carrier. Nucleic Acid Research 18, 378.CrossRefGoogle Scholar
GREGORY, R. D. (1991). Parasite epidemiology and host population growth: Heligmosomoides polygyrus (Nematoda) in enclosed wood mouse populations. Journal of Animal Ecology 60, 805821.CrossRefGoogle Scholar
GREGORY, R. D. (1992). On the interpretation of host–parasite ecology: Heligmosomoides polygyrus (Nematoda) in wild wood mouse (Apodemus sylvaticus) populations. Journal of Zoology, London 226, 109121.CrossRefGoogle Scholar
GREGORY, R. D., KEYMER, A. E. & CLARKE, J. R. (1990). Genetics, sex and exposure: the ecology of Heligmosomoides polygyrus (Nematoda) in the Wood Mouse. Journal of Animal Ecology 59, 363378.CrossRefGoogle Scholar
GREGORY, R. D., MONTGOMERY, S. S. J. & MONTGOMERY, W. I. (1992). Population biology of Heligmosomoides polygyrus (Nematoda) in the Wood Mouse. Journal of Animal Ecology 61, 749757.CrossRefGoogle Scholar
HOFFER, A. P. & HINTON, B. T. (1984). Morphological evidence for a blood-epididymis barrier and the effects of gossypol on its integrity. Biology of Reproduction 30, 9911004.CrossRefGoogle Scholar
HOGLUND, J., MORRISON, D. A., DIVINA, B. P., WILHELMSSON, E. & MATTSON, J. G. (2003). Phylogeny of Dictyocaulus (lungworms) from eight species of ruminants based on analyses of ribosoma RNA data. Parasitology 127, 179188.CrossRefGoogle Scholar
LEWIS, J. W. (1968). Studies on the helminth parasites of the long-tailed field mouse, Apodemus sylvaticus sylvaticus from Wales. Journal of Zoology, London 154, 287312.CrossRefGoogle Scholar
LEWIS, J. W. (1987). Helminth parasites of British rodents and insectivores. Mammalian Review 17, 8193.CrossRefGoogle Scholar
LI, P., CHAN, H. C., HE, B., SO, S. C., CHUNG, Y. W., SHANG, Q., ZHANG, Y. D. & ZHANG, Y. L. (2001). An antimicrobial peptide gene found in the male reproductive system of rats. Science 291, 17831785.CrossRefGoogle Scholar
LOCKHART, A. B., THRALL, P. H. & ANTONOVICS, J. (1996). Sexually transmited diseases in animals: ecological and evolutionary implications. Biological Reviews 71, 415471.CrossRefGoogle Scholar
MORAND, S. (1988). Cycle évolutif du Nemhelix bakeri Morand et Petter (Nematoda, Cosmocercidae), parasite de l'appareil de l'Helix aspersa Müller (Gastropoda, Helicidae). Canadian Journal of Zoology 66, 17961802.CrossRefGoogle Scholar
MORAND, S. & PETTER, A. J. (1986). Nemhelix bakeri n.gen., n.sp. (Nematoda: Cosmocercidae) parasite de l'appareil génital de Helix aspersa (Gastropoda: Helicidae) en France. Canadian Journal of Zoology 64, 20082011.Google Scholar
MORAND, S. & HOMMAY, G. (1990). Redescription de Agfa fles Dujardin 1845 (Nematoda: Agfidae) parasite de l'appareil génital de Limax cinereoniger Wolf (Gastropoda, Limacidae). Systematic Parasitology 15, 127132.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
SORVILLO, F., MORI, K., SEWAKE, W. & FISHMAN, L. (1983). Sexual transmission of Strongyloides stercoralis among homosexual men. British Journal of Venereal Diseases 59, 342.CrossRefGoogle Scholar