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Angiostrongylus vasorum from South America and Europe represent distinct lineages

  • R. JEFFERIES (a1) (a2), S. E. SHAW (a2), M. E. VINEY (a1) and E. R. MORGAN (a1) (a2)

Summary

Angiostrongylus vasorum is a nematode parasite of sylvan and domestic species of the family Canidae. It has a broad but patchy distribution worldwide, and there is evidence for geographical spread and increasing incidence of infection in recent years. While historically Angiostrongylus-like nematodes identified in dogs and foxes have been described as A. vasorum in Europe and Angiocaulus raillieti in South America, more recent taxonomic revision has amalgamated these into a single species, A. vasorum. Here we report, for the first time, the molecular characterization of isolates of A. vasorum from Germany, Portugal, Denmark and the United Kingdom on the basis of the mitochondrial COI gene and the second ribosomal internal transcribed spacer. When compared with isolates from Brazil, sequence analysis revealed 2 distinct genotypes. Estimated rates of evolution based on COI sequences for both nematode and host are consistent with the hypothesis that the presence of A. vasorum in South America is a result of an ancient evolutionary event. Angiostrongylus vasorum in South America potentially represents a separate species to that observed in Europe.

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Corresponding author

*Corresponding author: School of Biological Sciences, University of Bristol, BristolBS8 1UG, UK. Tel: +44 (0) 117 9287489. E-mail: Ryan.Jefferies@bristol.ac.uk

References

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Blouin, M. S. (2002). Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal for Parasitology 32, 527531.
Blouin, M. S., Yowell, C. A., Courtney, C. H. and Dame, J. B. (1998). Substitution bias, rapid saturation, and the use of mtDNA for nematode systematics. Molecular Biology and Evolution 15, 17191727.
Bolt, G., Monrad, J., Henriksen, P., Dietz, H. H., Koch, J., Bindseil, E. and Jensen, A. L. (1992). The fox (Vulpes vulpes) as a reservoir for canine angiostrongylosis in Denmark. Acta Veterinaria Scandinavica 33, 357362.
Bolt, G., Monrad, J., Koch, J. and Jensen, A. L. (1994). Canine angiostrongylosis: a review. Veterinary Record 135, 447452.
Bourque, A., Whitney, H. and Conboy, G. (2005). Angiostrongylus vasorum infection in a coyote (Canis latrans) from Newfoundland and Labrador. Canadian Journal of Wildlife Disease 41, 816819.
Bowles, J., Hope, M., Tiu, W. U., Liu, X. and McManus, D. P. (1993). Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum. Acta Tropica 55, 217229.
Bwangamoi, O. (1972). Angiostrongylus vasorum and other worms in dogs in Uganda. Veterinary Record 91, 267.
Caldeira, R. L., Carvalho, O. S., Mendonca, C. L. F. G., Graeff-Teixeira, C., Silva, M. C. F., Ben, R., Maurer, R., Lima, W. S. and Lenzi, H. L. (2003). Molecular differentiation of Angiostrongylus costaricensis, A. cantonensis and A. vasorum by polymerase chain reaction-restriction fragment length polymorphism. Memórias do Instituto Oswaldo Cruz 98, 10391043.
Costa, J. O., de Araujo Costa, H. M. and Guimaraes, M. P. (2003). Redescription of Angiostrongylus vasorum (Baillet, 1866) and systematic revision of species assigned to the genera Angiostrongylus Kamensky, 1905 and Angiocaulus Schulz, 1951. Revue de Médecine Vétérinaire 154, 916.
Dougherty, E. C. (1946). The genus Aelurostrongylus Cameron, 1927 (Nematoda: Metastrongylidae), and its relatives; with descriptions of Parafilaroides, gen. nov., and Angiostrongylus gubernaculatus, sp. nov. Proceedings of the Helminthological Society of Washington 13, 1626.
Faulkner, C. T., Patton, S., Munson, L., Johnson, E. M. and Coonan, T. J. (2001). Angiocaulus gubernaculatus in the Island Fox (Urocyon littoralis) from the California Channel Islands and comments on the diagnosis of Angiostrongylidae nematodes in canid and mustelid hosts. The Journal of Parasitology 87, 11741176.
Felsenstein, J. (2005). PHYLIP (Phylogeny Inference Package) Version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle, USA.
Fiorello, C. V., Robbins, R. G., Maffei, L. and Wade, S. E. (2006). Parasites of free-ranging small canids and felids in the Bolivian Chaco. Journal of Zoo and Wildlife Medicine 37, 130134.
Gasser, R. B., Chilton, N. B., Hoste, H. and Beveridge, I. (1993). Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Research 21, 25252526.
Goncalves, P. C. (1961). Angiostrongylus vasorum (Baillet, 1866), novo parasite do cao no Rio Grande do Sul (Brazil) (Nematoda: Metastrongyloidea). Revista da Faculdade de Agronomia Veterinaria da Universidade do Rio Grande do Sul 4, 3540.
Gortazar, C., Villafuerte, R., Lucientes, J. and Fernandez-de-Luco, D. (1998). Habitat related differences in helminth parasites of red foxes in the Ebro valley. Veterinary Parasitology 80, 7581.
Grisi, L. (1971). Ocorrência de Angiocaulus raillieti (Travassos, 1927) comb. n. em Canis familiaris L. (Nematoda, Protostrongylidae). Revista Brasileira de Biologia 31, 2732.
Guilhon, J. and Cens, B. (1973). Angiostrongylus vasorum (Baillet, 1866) etude biologique et morphologique. Annales de Parasitologie 48: 567596.
Gupta, B. P. and Sternberg, P. W. (2003). The draft genome sequence of the nematode Caenorhabditis briggsae, a companion to C. elegans. Genome Biology 4, 238.
Hu, M., Chilton, N. B. and Gasser, R. B. (2002). Long PCR-based amplification of the entire mitochondrial genome from single parasitic nematodes. Molecular and Cellular Probes 16, 261267.
Jeffery, R. A., Lankester, M. W., McGrath, M. J. and Whitney, H. G. (2004). Angiostrongylus vasorum and Crenosoma vulpis in red foxes (Vulpes vulpes) in Newfoundland, Canada. Canadian Journal of Zoology 82, 6674.
Koch, J. and Willesen, J. L. (2009). Canine pulmonary angiostrongylosis: an update. Veterinary Journal (in the Press). doi:10.1016/j.tvjl.2007.11.014
Lima, W. S., Guimaraes, M. P. and Lemos, I. S. (1994). Occurrence of Angiostrongylus vasorum in the lungs of the Brazilian Fox Dusicyon vetulus. Journal of Helminthology 68, 87.
Mattiucci, S. and Nascetti, G. (2006). Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: an update. Parasite 13, 99113.
Morgan, E. R., Shaw, S. E., Brennan, S. F., De Waal, T. D., Jones, B. R. and Mulcahy, G. (2005). Angiostrongylus vasorum: a real heartbreaker. Trends in Parasitology 21, 4951.
Morgan, E. R., Tomlinson, A., Hunter, S., Nichols, T., Roberts, E., Fox, M. T. and Taylor, M. A. (2008). Angiostrongylus vasorum and Eucoleus aerophilus in foxes (Vulpes vulpes) in Great Britain. Veterinary Parasitology 154, 4857.
Romstad, A., Gasser, R. B., Nansen, P., Polderman, A. M. and Chilton, N. B. (1998). Necator americanus (Nematoda: Anclyostomatidae) from Africa and Malaysia have different ITS-2 rRNA sequences. International Journal for Parasitology 28, 611615.
Rosen, L., Ash, L. R. and Wallace, G. D. (1970). Life history of the canine lungworm Angiostrongylus vasorum (Baillet). American Journal of Veterinary Research 31, 131143.
Segovia, J. M., Torres, J., Miquel, J., Llaneza, L. and Feliu, C. (2001). Helminths in the wolf, Canis lupus, from north-western Spain. Journal of Helminthology 75, 183192.
Sreter, T., Szell, Z., Marucci, G., Pozio, E. and Varga, I. (2003). Extraintestinal nematode infections of red foxes (Vulpes vulpes) in Hungary. Veterinary Parasitology 115, 329334.
Staebler, S., Ochs, H., Steffen, F., Naegeli, F., Borel, N., Sieber-Ruckstuhl, N. and Deplazes, P. (2005). Autochthone Infektionen mit Angiostrongylus vasorum bei Hunden in der Schweiz und Deutschland. Schweizer Archiv für Tierheilkunde 147, 121127.
Stein, L. D., Bao, Z., Blasiar, D., Blumenthal, T., Brent, M., Chen, N. S., Chinwalla, A., Clarke, L., Clee, C., Coghlan, A., Coulson, A., D'Eustachio, P., Fitch, D. H., Fulton, L. A., Fulton, R. E., Griffiths-Jones, S., Harris, T. W., Hillier, L. W., Kamath, R., Kuwabara, P. E., Mardis, E. R., Marra, M. A., Miner, T. L., Minx, P., Mullikin, J. C., Plumb, R. W., Rogers, J., Schein, J. E., Sohrmann, M., Spieth, J., Stajich, J. E., Wei, C., Willey, D., Wilson, R. K., Durbin, R., Waterston, R. H. (2003). The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biology 1, 166192.
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599.
Tebb, A. I., Johnson, V. S. and Irwin, P. J. (2007). Angiostrongylus vasorum (French heartworm) in a dog imported into Australia. Australian Veterinary Journal 85, 2328.
Travassos, L. (1927). Nematódeos novos. Boletim Biologico Sao Paulo 6, 5261.
Wang, X., Tedford, R. H., Van Valkenburgh, B. and Wayne, R. K. (2004). Ancestry: Evolutionary history, molecular systematics, and evolutionary ecology of Canidae, In The Biology and Conservation of Wild Canids (ed.MacDonald, D. W. and Sillero-Zubiri, C.), pp. 3954. Oxford University Press, Oxford, UK.
Williams, J. F., Lindemann, B., Padgett, G. A. and Smith, O. L. (1985). Angiostrongylosis in a greyhound. Journal of the American Veterinary Medical Association 186, 11011103.

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Angiostrongylus vasorum from South America and Europe represent distinct lineages

  • R. JEFFERIES (a1) (a2), S. E. SHAW (a2), M. E. VINEY (a1) and E. R. MORGAN (a1) (a2)

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