Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-24T18:58:10.160Z Has data issue: false hasContentIssue false
  • English
  • Français

A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes

Published online by Cambridge University Press:  11 December 2006

M. NAKAO ,
D. P. McMANUS ,
P. M. SCHANTZ ,
P. S. CRAIG  and
A. ITO
M. NAKAO*
Affiliation:
Department of Parasitology, Asahikawa Medical College, Asahikawa, Hokkaido 078-8510, Japan
D. P. McMANUS
Affiliation:
Molecular Parasitology Laboratory, The Queensland Institute of Medical Research and the University ofQueensland, Brisbane, Queensland 4029, Australia
P. M. SCHANTZ
Affiliation:
Division of Parasitic Diseases, National Centers for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA 30341, USA
P. S. CRAIG
Affiliation:
Cestode Zoonoses Research Group, Bioscience Research Institute and School of Environment and Life Sciences, University of Salford, Great Manchester M5 4WT, UK
A. ITO
Affiliation:
Department of Parasitology, Asahikawa Medical College, Asahikawa, Hokkaido 078-8510, Japan
*
*Corresponding author: Department of Parasitology, Asahikawa Medical College, Asahikawa, Hokkaido 078-8510, Japan. Tel: +81 166 68 2422. Fax: +81 166 68 2429. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Taxonomic revision by molecular phylogeny is needed to categorize members of the genus Echinococcus (Cestoda: Taeniidae). We have reconstructed the phylogenetic relationships of E. oligarthrus, E. vogeli, E. multilocularis, E. shiquicus, E. equinus, E. ortleppi, E. granulosus sensu stricto and 3 genotypes of E. granulosus sensu lato (G6, G7 and G8) from their complete mitochondrial genomes. Maximum likelihood and partitioned Bayesian analyses using concatenated data sets of nucleotide and amino acid sequences depicted phylogenetic trees with the same topology. The 3 E. granulosus genotypes corresponding to the camel, pig, and cervid strains were monophyletic, and their high level of genetic similarity supported taxonomic species unification of these genotypes into E. canadensis. Sister species relationships were confirmed between E. ortleppi and E. canadensis, and between E. multilocularis and E. shiquicus, regardless of the analytical approach employed. The basal positions of the phylogenetic tree were occupied by the neotropical endemic species, E. oligarthrus and E. vogeli, whose definitive hosts are derived from carnivores that immigrated from North America after the formation of the Panamanian land bridge. Host-parasite co-evolution comparisons suggest that the ancestral homeland of Echinococcus was North America or Asia, depending on whether the ancestral definitive hosts were canids or felids.

Keywords

Echinococcusmitochondrial genomephylogenytaxonomic revision
Type
Research Article
Information
Parasitology , Volume 134 , Issue 5 , May 2006 , pp. 713 - 722
Copyright
Copyright © Cambridge University Press 2006

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

Abascal, F., Zardoya, R. and Posada, D. (2005). ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104–2105.CrossRefGoogle ScholarPubMed
Bowles, J., Blair, D. and McManus, D. P. (1994). Molecular genetic characterization of the cervid strain (‘northern form’) of Echinococcus granulosus. Parasitology 109, 215–221.CrossRefGoogle ScholarPubMed
Bowles, J., Blair, D. and McManus, D. P. (1995). A molecular phylogeny of the genus Echinococcus. Parasitology 110, 317–328.CrossRefGoogle ScholarPubMed
Brown, W. M., George, M. Jr. and Wilson, A. C. (1979). Rapid evolution of animal mitochondrial DNA. Proceedings of the National Academy of Sciences, USA 76, 1967–1971.Google Scholar
Cameron, T. W. M. (1960). The incidence and diagnosis of hydatid cyst in Canada. Echinococcus granulosus var. canadensis. Parassitologia 2, 381–390.Google Scholar
D'Alessandro, A., Rausch, R. L., Morales, G. A., Collet, S. and Angel, D. (1981). Echinococcus infections in Colombian animals. The American Journal of Tropical Medicine and Hygiene 30, 1263–1276.CrossRefGoogle ScholarPubMed
Eckert, J., Thompson, R. C. A., Lymbery, A. J., Pawlowski, Z. S., Gottstein, B. and Morgan, U. M. (1993). Further evidence for the occurrence of a distinct strain of Echinococcus granulosus in European pigs. Parasitology Research 79, 42–48.CrossRefGoogle ScholarPubMed
Felsenstein, J. (2005). PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author via the internet. Department of Genome Sciences, University of Washington, Seattle, Washington, USA.Google Scholar
Haag, K. L., Araujo, A. M., Gottstein, B., Siles-Lucas, M., Thompson, R. C. A. and Zaha, A. (1999). Breeding systems in Echinococcus granulosus (Cestoda; Taeniidae): selfing or outcrossing? Parasitology 118, 63–71.Google Scholar
Hoberg, E. P., Jones, A., Rausch, R. L., Eom, K. S. and Gardner, S. L. (2000). A phylogenetic hypothesis for species of the genus Taenia (Eucestoda: Taeniidae). The Journal of Parasitology 86, 89–98.CrossRefGoogle ScholarPubMed
Hoberg, E. P., Alkire, N. L., de Queiroz, A. and Jones, A. (2001). Out of Africa: origins of the Taenia tapeworms in humans. Proceedings of the Royal Society of London, B 268, 781–787.CrossRefGoogle ScholarPubMed
Johnson, W. E., Eizirik, E., Pecon-Slattery, J., Murphy, W. J., Antunes, A., Teeling, E. and O'Brien, S. J. (2006). The late Miocene radiation of modern Felidae: a genetic assessment. Science 311, 73–77.Google Scholar
Kumaratilake, L. M. and Thompson, R. C. A. (1982). A review of the taxonomy and speciation of the genus Echinococcus Rudolphi 1801. Zeitschrift für Parasitenkunde 68, 121–146.CrossRefGoogle ScholarPubMed
Lavikainen, A., Lehtinen, M. J., Ågren, E. and Meri, S. (2005). Phylogeny of the Fennoscandian cervid strain of Echinococcus granulosus. Bulletin of the Scandinavian-Baltic Society for Parasitology 14, 92.Google Scholar
Lavikainen, A., Lehtinen, M. J., Meri, T., Hirvela-Koski, V. and Meri, S. (2003). Molecular genetic characterization of the Fennoscandian cervid strain, a new genotypic group (G10) of Echinococcus granulosus. Parasitology 127, 207–215.CrossRefGoogle Scholar
Lavikainen, A., Lehtinen, M. J., Laaksonen, S., Ågren, E., Oksanen, A. and Meri, S. (2006). Molecular characterization of Echinococcus isolates of cervid origin from Finland and Sweden. Parasitology 133, 565–570.Google Scholar
Le, T. H., Pearson, M. S., Blair, D., Dai, N., Zhang, L. H. and McManus, D. P. (2002). Complete mitochondrial genomes confirm the distinctiveness of the horse-dog and sheep-dog strains of Echinococcus granulosus. Parasitology 124, 97–112.CrossRefGoogle ScholarPubMed
Lopez-Neyra, C. R. and Soler Planas, M. A. (1943). Revision del genero Echinococcus Rud y description de una especie nuéva Parasita intestinal del perro en Almeria. Revista ibérica de parasitología 3, 169–194.Google Scholar
Lymbery, A. J. and Thompson, R. C. A. (1996). Species of Echinococcus: pattern and process. Parasitology Today 12, 486–491.CrossRefGoogle ScholarPubMed
Maddison, D. R. and Maddison, W. P. (2000). MacClade 4: analysis of phylogeny and character evolution. Sinauer Associates, Sunderland, Massachusetts, USA.Google Scholar
Marshall, L. G., Webb, S. D., Sepkoski, J. J. and Raup, D. M. (1982). Mammalian evolution and the Great American Interchange. Science 215, 1351–1357.CrossRefGoogle ScholarPubMed
McManus, D. P. and Thompson, R. C. A. (2003). Molecular epidemiology of cystic echinococcosis. Parasitology 127 (Suppl.), S37–S51.CrossRefGoogle ScholarPubMed
Mueller, R. L., Macey, J. R., Jaekel, M., Wake, D. B. and Boore, J. L. (2004). Morphological homoplasy, life history evolution, and historical biogeography of plethodontid salamanders inferred from complete mitochondrial genomes. Proceedings of the National Academy of Sciences, USA 101, 13820–13825.CrossRefGoogle ScholarPubMed
Murphy, W. J., Eizirik, E., O'Brien, S. J., Madsen, O., Scally, M., Douady, C. J., Teeling, E., Ryder, O. A., Stanhope, M. J., de Jong, W. W. and Springer, M. S. (2001). Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294, 2348–2351.Google Scholar
Nakao, M., Okamoto, M., Sako, Y., Yamasaki, H., Nakaya, K. and Ito, A. (2002 a). A phylogenetic hypothesis for the distribution of two genotypes of the pig tapeworm Taenia solium worldwide. Parasitology 124, 657–662.Google Scholar
Nakao, M., Sako, Y. and Ito, A. (2003). The mitochondrial genome of the tapeworm Taenia solium: a finding of the abbreviated stop codon U. The Journal of Parasitology 89, 633–635.Google Scholar
Nakao, M., Sako, Y., Yokoyama, N., Fukunaga, M. and Ito, A. (2000). Mitochondrial genetic code in cestodes. Molecular and Biochemical Parasitology 111, 415–424.CrossRefGoogle ScholarPubMed
Nakao, M., Yokoyama, N., Sako, Y., Fukunaga, M. and Ito, A. (2002 b). The complete mitochondrial DNA sequence of the cestode Echinococcus multilocularis (Cyclophyllidea: Taeniidae). Mitochondrion 1, 497–509.CrossRefGoogle ScholarPubMed
Nylander, J. A., Ronquist, F., Huelsenbeck, J. P. and Nieves-Aldrey, J. L. (2004). Bayesian phylogenetic analysis of combined data. Systematic Biology 53, 47–67.Google Scholar
Ortlepp, R. J. (1937). South African Helminths. Part I. The Onderstepoort Journal of Veterinary Science and Animal Industry 9, 311–336.Google Scholar
Posada, D. and Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Rausch, R. L. (1967). A consideration of infraspecific categories in the genus Echinococcus Rudolphi, 1801 (Cestoda: Taeniidae). The Journal of Parasitology 53, 484–491.Google Scholar
Rausch, R. L. and Bernstein, J. J. (1972). Echinococcus vogeli sp. n. (Cestoda: Taeniidae) from the bush dog, Speothos venaticus (Lund). Zeitschrift für Tropenmedizin und Parasitologie 23, 25–34.Google Scholar
Rice, P., Longden, I. and Bleasby, A. (2000). EMBOSS: The European Molecular Biology Open Software Suite. Trends in Genetics 16, 276–277.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Scott, J. C., Stefaniak, J., Pawlowski, Z. S. and McManus, D. P. (1997). Molecular genetic analysis of human cystic hydatid cases from Poland: identification of a new genotypic group (G9) of Echinococcus granulosus. Parasitology 114, 37–43.Google Scholar
Smyth, J. D. and Smyth, M. M. (1964). Natural and experimental hosts of Echinococcus granulosus and E. multilocularis, with comments on the genetics of speciation in the genus Echinococcus. Parasitology 54, 493–514.CrossRefGoogle Scholar
Sweatman, G. K. and Williams, R. J. (1963). Comparative studies on the biology and morphology of Echinococcus granulosus from domestic livestock, moose and reindeer. Parasitology 53, 339–390.Google Scholar
Swofford, D. L. (2002). PAUP*: phylogenetic analysis using parsimony (and other methods) 4.0 beta. Sinauer Associates, Sunderland, Massachusetts, USA.Google Scholar
Telford, M. J., Herniou, E. A, Russell, R. B. and Littlewood, D. T. (2000). Changes in mitochondrial genetic codes as phylogenetic characters: two examples from the flatworms. Proceedings of the National Academy of Sciences, USA 97, 11359–11364.CrossRefGoogle ScholarPubMed
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.Google Scholar
Thompson, R. C. A., Boxell, A. C., Ralston, B. J., Constantine, C. C., Hobbs, R. P., Shury, T. and Olson, M. E. (2006). Molecular and morphological characterization of Echinococcus in cervids from North America. Parasitology 132, 439–447.CrossRefGoogle ScholarPubMed
Thompson, R. C. A., Lymbery, A. J. and Constantine, C. C. (1995). Variation in Echinococcus: towards a taxonomic revision of the genus. Advances in Parasitology 35, 145–176.CrossRefGoogle ScholarPubMed
Thompson, R. C. A. and McManus, D. P. (2003). Towards a taxonomic revision of the genus Echinococcus. Trends in Parasitology 18, 452–457.CrossRefGoogle Scholar
Verster, A. J. M. (1965). Review of Echinococcus species in South Africa. The Onderstepoort Journal of Veterinary Research 32, 7–118.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 Biology and Conservation of Wild Canids (ed. MacDonald, D. W. and Sillero-Zubiri, C.), pp. 39–54. Oxford University Press, Oxford.CrossRefGoogle Scholar
Wayne, R. K., Geffen, E., Girman, D. J., Koepfli, K. P., Lau, L. M. and Marshall, C. R. (1997). Molecular systematics of the Canidae. Systematic Biology 46, 622–653.Google Scholar
Webster, G. A. and Cameron, T. W. M. (1961). Observations on experimental infections with Echinococcus in rodents. Canadian Journal of Zoology 39, 877–891.CrossRefGoogle Scholar
Williams, R. J. and Sweatman, G. K. (1963). On the transmission, biology and morphology of Echinococcus granulosus equinus, a new subspecies of hydatid tapeworm in horses in Great Britain. Parasitology 53, 391–407.Google Scholar
Xiao, N., Qiu, J., Nakao, M., Li, T., Yang, W., Chen, X., Schantz, P. M., Craig, P. S. and Ito, A. (2005). Echinococcus shiquicus n. sp., a taeniid cestode from Tibetan fox and plateau pika in China. International Journal for Parasitology 35, 693–701.CrossRefGoogle Scholar