Hostname: page-component-745bb68f8f-grxwn Total loading time: 0 Render date: 2025-02-04T17:21:12.737Z Has data issue: false hasContentIssue false
  • English
  • Français

Angiostrongylus vasorum from South America and Europe represent distinct lineages

Published online by Cambridge University Press:  07 January 2009

R. JEFFERIES ,
S. E. SHAW ,
M. E. VINEY  and
E. R. MORGAN
R. JEFFERIES*
Affiliation:
School of Biological Sciences, University of Bristol, BristolBS8 1UG, UK Department of Clinical Veterinary Sciences, University of Bristol, Langford, North SomersetBS40 5DU, UK
S. E. SHAW
Affiliation:
Department of Clinical Veterinary Sciences, University of Bristol, Langford, North SomersetBS40 5DU, UK
M. E. VINEY
Affiliation:
School of Biological Sciences, University of Bristol, BristolBS8 1UG, UK
E. R. MORGAN
Affiliation:
School of Biological Sciences, University of Bristol, BristolBS8 1UG, UK Department of Clinical Veterinary Sciences, University of Bristol, Langford, North SomersetBS40 5DU, UK
*
*Corresponding author: School of Biological Sciences, University of Bristol, BristolBS8 1UG, UK. Tel: +44 (0) 117 9287489. E-mail: Ryan.Jefferies@bristol.ac.uk
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

Angiostrongylus vasorumAngiocaulus raillietiBrazilco-evolutionCOIdogEuropefoxITS-2nematodephylogenetics
Type
Research Article
Information
Parasitology , Volume 136 , Issue 1 , January 2009 , pp. 107 - 115
Copyright
Copyright © 2009 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

Blouin, M. S. (2002). Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal for Parasitology 32, 527–531.CrossRefGoogle ScholarPubMed
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, 1719–1727.Google Scholar
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, 357–362.CrossRefGoogle ScholarPubMed
Bolt, G., Monrad, J., Koch, J. and Jensen, A. L. (1994). Canine angiostrongylosis: a review. Veterinary Record 135, 447–452.Google Scholar
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, 816–819.CrossRefGoogle Scholar
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, 217–229.CrossRefGoogle ScholarPubMed
Bwangamoi, O. (1972). Angiostrongylus vasorum and other worms in dogs in Uganda. Veterinary Record 91, 267.CrossRefGoogle ScholarPubMed
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, 1039–1043.CrossRefGoogle Scholar
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, 9–16.Google Scholar
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, 16–26.Google ScholarPubMed
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, 1174–1176.CrossRefGoogle ScholarPubMed
Felsenstein, J. (2005). PHYLIP (Phylogeny Inference Package) Version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle, USA.Google Scholar
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, 130–134.CrossRefGoogle ScholarPubMed
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, 2525–2526.CrossRefGoogle ScholarPubMed
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, 35–40.Google Scholar
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, 75–81.CrossRefGoogle ScholarPubMed
Grisi, L. (1971). Ocorrência de Angiocaulus raillieti (Travassos, 1927) comb. n. em Canis familiaris L. (Nematoda, Protostrongylidae). Revista Brasileira de Biologia 31, 27–32.Google Scholar
Guilhon, J. and Cens, B. (1973). Angiostrongylus vasorum (Baillet, 1866) etude biologique et morphologique. Annales de Parasitologie 48: 567–596.Google Scholar
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.CrossRefGoogle ScholarPubMed
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, 261–267.Google Scholar
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, 66–74.CrossRefGoogle Scholar
Koch, J. and Willesen, J. L. (2009). Canine pulmonary angiostrongylosis: an update. Veterinary Journal (in the Press). doi:10.1016/j.tvjl.2007.11.014CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Mattiucci, S. and Nascetti, G. (2006). Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: an update. Parasite 13, 99–113.Google Scholar
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, 49–51.Google Scholar
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, 48–57.Google Scholar
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, 611–615.Google Scholar
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, 131–143.Google Scholar
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, 183–192.Google ScholarPubMed
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, 329–334.CrossRefGoogle ScholarPubMed
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, 121–127.Google Scholar
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, 166–192.CrossRefGoogle ScholarPubMed
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, 1596–1599.CrossRefGoogle ScholarPubMed
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, 23–28.CrossRefGoogle Scholar
Travassos, L. (1927). Nematódeos novos. Boletim Biologico Sao Paulo 6, 52–61.Google Scholar
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. 39–54. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
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, 1101–1103.Google Scholar