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A phylogeny of members of the family Taeniidae based on the mitochondrial cox1 and nad1 gene data

  • A. LAVIKAINEN (a1), V. HAUKISALMI (a2), M. J. LEHTINEN (a1), H. HENTTONEN (a2), A. OKSANEN (a3) and S. MERI (a1) (a4)...

The cestode family Taeniidae consists of 2 genera, Taenia and Echinococcus, which both have been the focus of intensive taxonomic and epidemiological studies because of their zoonotic importance. However, a comprehensive molecular phylogeny of this family has yet to be reconstructed. In this study, 54 isolates representing 9 Taenia species were characterized using DNA sequences in the mitochondrial cytochrome c oxidase subunit 1 (cox1) and NADH dehydrogenase subunit 1 (nad1) genes. Phylogenetic relationships within the family Taeniidae were inferred by combining cox1 and nad1 sequence data of the present and previous studies. In the phylogenetic analysis, the genus Echinococcus was shown to be monophyletic, but Taenia proved to be paraphyletic due to the position of T. mustelae as a probable sister taxon of Echinococcus. This indicates that T. mustelae should form a genus of its own. Taenia ovis krabbei was placed distant from T. ovis ovis, as a sister taxon of T. multiceps, supporting its recognition as a distinct species, T. krabbei. High intraspecific sequence variation within both T. polyacantha and T. taeniaeformis suggests the existence of cryptic sister species.

Corresponding author
*Corresponding author: Department of Bacteriology and Immunology, Haartman Institute, P.O. Box 21, FI-00014 University of Helsinki, Finland. Tel: +358919126891. Fax: +358919126382. E-mail:
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Abuladze, K. I. (1964). Essentials of Cestodology. Vol IV. Taeniata of Animals and Man and Diseases Caused by them (ed .Skrjabin, K. I.). Nauka, Moskow. English translation (1970), Israel Program of Scientific Translations, Jerusalem.
Azuma, H., Okamoto, M., Oku, Y. and Kamiya, M. (1995). Intraspecific variation of Taenia taeniaeformis as determined by various criteria. Parasitology Research 81, 103108.
Bessonov, A. S., Movsessian, S. O. and Abuladze, K. I. (1994). On the classification and validity of superspecies taxons of the cestodes of the suborder Taeniata Skrjabin et Schulz, 1937. Helminthologia 31, 6771.
Bowles, J., Blair, D. and McManus, D. P. (1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165174.
Bowles, J., Blair, D. and McManus, D. P. (1995). A molecular phylogeny of the genus Echinococcus. Parasitology 110, 317328.
Bowles, J. and McManus, D. P. (1993). NADH dehydrogenase 1 gene sequences compared for species and strains of the genus Echinococcus. International Journal for Parasitology 23, 969972.
Bowles, J. and McManus, D. P. (1994). Genetic characterization of Asian Taenia, a newly described taeniid cestode of humans. American Journal of Tropical Medicine and Hygiene 50, 3344.
Chilton, N. B., Gasser, R. B. and Beveridge, I. (1997). Phylogenetic relationships of Australian strongyloid nematodes inferred from ribosomal DNA sequence data. International Journal for Parasitology 27, 14811494.
Eckert, J., Gemmell, M. A., Meslin, F.-X. and Pawlowski, Z. S. (eds) (2001). WHO/OIE Manual on Echinococcosis in Humans and Animals: a Public Health Problem of Global Concern. World Organization for Animal Health and World Health Organization, Paris, France.
Eckert, K. A. and Kunkel, T. A. (1991). DNA polymerase fidelity and the polymerase chain reaction. PCR Methods and Applications 1, 1724.
Freeman, R. S. (1956). Life history studies on Taenia mustelae Gmelin, 1790 and the taxonomy of certain taenioid cestodes from Mustelidae. Canadian Journal of Zoology 34, 219242.
Gasser, R. B., Zhu, X. and McManus, D. P. (1999). NADH dehydrogenase subunit 1 and cytochrome c oxidase subunit I sequences compared for members of the genus Taenia (Cestoda). International Journal for Parasitology 29, 19651970.
Harrison, R. G. (1989). Animal mitochondrial DNA as a genetic marker in population and evolutionary biology. Trends in Ecology & Evolution 4, 611.
Hoberg, E. P. (2002). Taenia tapeworms: their biology, evolution and socioeconomic significance. Microbes and Infection 4, 859866.
Hoberg, E. P. (2006). Phylogeny of Taenia: Species definitions and origins of human parasites. Parasitology International 55, S23S30. doi: 10.1016/jparint.2005.11.049.
Hoberg, E. P., Alkire, N. L., de Queiroz, A. and Jones, A. (2001). Out of Africa: orgins of the Taenia tapeworms in humans. Proceedings of the Royal Society of London, B 268, 781787. doi: 10.1098/rspb.2000.1579.
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, 8998.
Hüttner, M., Nakao, M., Wassermann, T., Siefert, L., Boomker, J. D. F., Dinkel, A., Sako, Y., Mackenstedt, U., Romig, T. and Ito, A. (2008). Genetic characterization and phylogenetic position of Echinococcus felidis Ortlepp, 1937 (Cestoda: Taeniidae) from the African lion. International Journal for Parasitology 38, 861868. doi: 10.1016/j.ijpara.2007.10.013.
Iwaki, T., Nonaka, N., Okamoto, M., Oku, Y. and Kamiya, M. (1994). Developmental and morphological characteristics of Taenia taeniaeformis (Batsch, 1786) in Clethrionomys rufocanus bedfordiae and Rattus norvegicus from different geographical locations. The Journal of Parasitology 80, 461467.
Jeon, H. K., Lee, K. H., Kim, K. H., Hwang, U. W. and Eom, K. S. (2005). Complete sequence and structure of the mitochondrial genome of the human tapeworm, Taenia asiatica (Platyhelminthes; Cestoda). Parasitology 130, 717726. doi: 10.1017/S0031182004007164.
Kedra, A. H., Tkach, V. V., Swiderski, Z. and Pawlowski, Z. (2001). Intraspecific variability among NAHD dehydrogenase subunit 1 sequences of Taenia hydatigena. Parasitology International 50, 145148.
Korniushin, V. V. and Sharpilo, L. D. (1986). Novyi rod teniid (Cestoda, Taeniidae) – parazitov kun'ikh. Vestnik zoologii 20, 1016.
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, 565570. doi: 10.1017/S0031182006000667.
Lavikainen, A., Lehtinen, M. J., Meri, T., Hirvelä-Koski, V. and Meri, S. (2003). Molecular genetic characterization of the Fennoscandian cervid strain, a new genotypic group (G10) of Echinococcus granulosus. Parasitology 127, 207215. doi: 10.1017/S0031182003003780.
Le, T. H., Blair, D., Agatsuma, T., Humair, P. F., Campbell, N. J., Iwagami, M., Littlewood, D. T., Peacock, B., Johnston, D. A., Bartley, J., Rollinson, D., Herniou, E. A., Zarlenga, D. S. and McManus, D. P. (2000). Phylogenies inferred from mitochondrial gene orders – a cautionary tale from the parasitic flatworms. Molecular Biology and Evolution 17, 11231125.
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, 97112. doi: 10.1017/S0031182001008976.
Locker, B. (1955). The identification of Taenia tenuicollis Rudolphi, 1819, in North America. The Journal of Parasitology 41, 5156.
Loos-Frank, B. (2000). An up-date of Verster's (1969) ‘Taxonomic revision of the genus Taenia Linnaeus’ (Cestoda) in table format. Systematic Parasitology 45, 155183.
Moks, E., Jõgisalu, I., Valdmann, H. and Saarma, U. (2008). First report of Echinococcus granulosus G8 in Eurasia and reappraisal of the phylogenetic relationships of ‘genotypes’ G5-G10. Parasitology 135, 647654. doi: 10.1017/S0031182008004198.
Moore, J. and Brooks, D. R. (1987). Asexual reproduction in cestodes (Cyclophyllidea: Taeniidae): Ecological and phylogenetic influences. Evolution 41, 882891.
Nakao, M., McManus, D. P., Schantz, P. M., Craig, P. S. and Ito, A. (2007). A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134, 713722. doi: 10.1017/S0031182006001934.
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, 633635.
Nakao, M., Sako, Y., Yokoyamo, N., Fukunaga, M. and Ito, A. (2000). Mitochondrial genetic code in cestode. Molecular and Biochemical Parasitology 111, 415424.
Nakao, M., Yokoyama, N., Sako, Y., Fukunaga, M. and Ito, A. (2002). The complete mitochondrial DNA sequence of the cestode Echinococcus multilocularis (Cyclophyllidea: Taeniidae). Mitochondrion 1, 497509.
von Nickisch-Rosenegk, M., Brown, W. M. and Boore, J. L. (2001). Complete sequence of the mitochondrial genome of the tapeworm Hymenolepis diminuta: gene arrangements indicate that Platyhelminths are Eutrochozoans. Molecular Biology and Evolution 18, 721730.
von Nickisch-Rosenegk, M., Silva-Gonzalez, R. and Lucius, R. (1999). Modification of universal 12S primers for specific amplification of contaminated Taenia spp. (Cestoda) gDNA enabling phylogenetic studies. Parasitology Research 85, 819825.
Obwaller, A., Schneider, R., Walochnik, J., Gollackner, B., Deutz, A., Janitschke, K., Aspöck, H. and Auer, H. (2004). Echinococcus granulosus strain differentiation based on sequence heterogeneity in mitochondrial genes of cytochrome c oxidase-1 and NADH dehydrogenase-1. Parasitology 128, 569575. doi: 10.1017/S0031182004004871.
Okamoto, M., Bessho, Y., Kamiya, M., Kurosawa, T. and Horii, T. (1995 a). Phylogenetic relationships within Taenia taeniaeformis variants and other taeniid cestodes inferred from the nucleotide sequence of the cytochrome c oxidase subunit I gene. Parasitology Research 81, 415458.
Okamoto, M., Ito, A., Kurosawa, T., Oku, Y., Kamiya, M. and Agatsuma, T. (1995 b). Intraspecific variation of isoenzymes in Taenia taeniaeformis. International Journal for Parasitology 25, 221228.
Posanda, D. and Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817818.
Priemer, J., Krone, O. and Schuster, R. (2002). Taenia krabbei (Cestoda: Cyclophyllidea) in Germany and its delimitation from T. ovis. Zoologischer Anzeiger 241, 333337.
de Queiroz, A. and Alkire, N. L. (1998). The phylogenetic placement of Taenia cestodes that parasitize humans. The Journal of Parasitology 84, 379383.
Rausch, R. L. and Fay, F. H. (1988). Postoncospheral development and cycle of Taenia polyacantha Leuckart, 1856 (Cestoda: Taeniidae). Annales de Parasitologie Humaine et Comparée 63, 263277 and 334348.
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680.
Verster, A. (1969). A taxonomic revision of the genus Taenia Linnaeus, 1758 s. str. Onderstepoort Journal of Veterinary Research 36, 358.
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, 693701. doi: 10.1016/j.ijpara.2005.01.003.
Zhang, D.-X. and Hewitt, G. M. (1996). Nuclear integrations: challenges for mitochondrial DNA markers. Trends in Ecology & Evolution 11, 247251.
Zhang, L., Hu, M., Jones, A., Alsopp, B. A., Beveridge, I., Schindler, A. R. and Gasser, R. B. (2007). Characterization of Taenia madoquae and Taenia regis from carnivores in Kenya using genetic markers in nuclear and mitochondrial DNA, and their relationships with other selected taeniids. Molecular and Cellular Probes 21, 379385. doi: 10.1016/j.mcp.2007.05.003.
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