Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-25T07:42:51.689Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  21 October 2008

A. LAVIKAINEN*
Affiliation:
Department of Bacteriology and Immunology, Haartman Institute, P.O. Box 21, FI-00014 University of Helsinki, Finland
V. HAUKISALMI
Affiliation:
Vantaa Research Unit, Finnish Forest Research Institute, P.O. Box 18, FI-01301 Vantaa, Finland
M. J. LEHTINEN
Affiliation:
Department of Bacteriology and Immunology, Haartman Institute, P.O. Box 21, FI-00014 University of Helsinki, Finland
H. HENTTONEN
Affiliation:
Vantaa Research Unit, Finnish Forest Research Institute, P.O. Box 18, FI-01301 Vantaa, Finland
A. OKSANEN
Affiliation:
Fish and Wildlife Health Research Unit, Finnish Food Safety Authority Evira, P.O. Box 517, FI-90101 Oulu, Finland
S. MERI
Affiliation:
Department of Bacteriology and Immunology, Haartman Institute, P.O. Box 21, FI-00014 University of Helsinki, Finland Helsinki University Central Hospital, P.O. Box 400, FI-00029 HUS, Finland
*
*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: [email protected]

Summary

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.

Type
Original Articles
Copyright
Copyright © 2008 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

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.Google Scholar
Azuma, H., Okamoto, M., Oku, Y. and Kamiya, M. (1995). Intraspecific variation of Taenia taeniaeformis as determined by various criteria. Parasitology Research 81, 103108.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
Bowles, J., Blair, D. and McManus, D. P. (1995). A molecular phylogeny of the genus Echinococcus. Parasitology 110, 317328.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
Eckert, K. A. and Kunkel, T. A. (1991). DNA polymerase fidelity and the polymerase chain reaction. PCR Methods and Applications 1, 1724.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Harrison, R. G. (1989). Animal mitochondrial DNA as a genetic marker in population and evolutionary biology. Trends in Ecology & Evolution 4, 611.CrossRefGoogle ScholarPubMed
Hoberg, E. P. (2002). Taenia tapeworms: their biology, evolution and socioeconomic significance. Microbes and Infection 4, 859866.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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, 8998.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Korniushin, V. V. and Sharpilo, L. D. (1986). Novyi rod teniid (Cestoda, Taeniidae) – parazitov kun'ikh. Vestnik zoologii 20, 1016.Google 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, 565570. doi: 10.1017/S0031182006000667.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle 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, 97112. doi: 10.1017/S0031182001008976.CrossRefGoogle ScholarPubMed
Locker, B. (1955). The identification of Taenia tenuicollis Rudolphi, 1819, in North America. The Journal of Parasitology 41, 5156.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Moore, J. and Brooks, D. R. (1987). Asexual reproduction in cestodes (Cyclophyllidea: Taeniidae): Ecological and phylogenetic influences. Evolution 41, 882891.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Nakao, M., Sako, Y., Yokoyamo, N., Fukunaga, M. and Ito, A. (2000). Mitochondrial genetic code in cestode. Molecular and Biochemical Parasitology 111, 415424.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Posanda, D. and Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817818.CrossRefGoogle Scholar
Priemer, J., Krone, O. and Schuster, R. (2002). Taenia krabbei (Cestoda: Cyclophyllidea) in Germany and its delimitation from T. ovis. Zoologischer Anzeiger 241, 333337.CrossRefGoogle Scholar
de Queiroz, A. and Alkire, N. L. (1998). The phylogenetic placement of Taenia cestodes that parasitize humans. The Journal of Parasitology 84, 379383.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Verster, A. (1969). A taxonomic revision of the genus Taenia Linnaeus, 1758 s. str. Onderstepoort Journal of Veterinary Research 36, 358.Google ScholarPubMed
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.CrossRefGoogle Scholar
Zhang, D.-X. and Hewitt, G. M. (1996). Nuclear integrations: challenges for mitochondrial DNA markers. Trends in Ecology & Evolution 11, 247251.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed