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Molecular identification of Taenia spp. in the Eurasian lynx (Lynx lynx) from Finland

  • A. LAVIKAINEN (a1), V. HAUKISALMI (a2) (a3), G. DEKSNE (a4) (a5), K. HOLMALA (a6), M. LEJEUNE (a7), M. ISOMURSU (a8), P. JOKELAINEN (a9), A. NÄREAHO (a9), J. LAAKKONEN (a9), E. P. HOBERG (a10) and A. SUKURA (a9)...
Summary

Cestodes of the genus Taenia are parasites of mammals, with mainly carnivores as definitive and herbivores as intermediate hosts. Various medium-sized cats, Lynx spp., are involved in the life cycles of several species of Taenia. The aim of the present study was to identify Taenia tapeworms in the Eurasian lynx (Lynx lynx) from Finland. In total, 135 tapeworms from 72 lynx were subjected to molecular identification based on sequences of 2 mtDNA regions, the cytochrome c oxidase subunit 1 and the NADH dehydrogenase subunit 1 genes. Available morphological characters of the rostellar hooks and strobila were compared. Two species of Taenia were found: T. laticollis (127 samples) and an unknown Taenia sp. (5 samples). The latter could not be identified to species based on mtDNA, and the rostellar hooks were short relative to those described among other Taenia spp. recorded in felids from the Holarctic region. In the phylogenetic analyses of mtDNA sequences, T. laticollis was placed as a sister species of T. macrocystis, and the unknown Taenia sp. was closely related to T. hydatigena and T. regis. Our analyses suggest that these distinct taeniid tapeworms represent a putative new species of Taenia. The only currently recognized definitive host is L. lynx and the intermediate host is unknown.

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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: antti.lavikainen@helsinki.fi
References
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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.
Al-Sabi, M. N. S. and Kapel, C. M. O. (2011). Multiplex PCR identification of Taenia spp. in rodents and carnivores. Parasitology Research 109, 12931298. doi: 10.1007/s00436-011-2373-9.
Bagrade, G., Vismanis, K., Kirjušina, M. and Ozolinš, J. (2003). Preliminary results on the helminthofauna of the Eurasian lynx (Lynx lynx) in Latvia. Acta Zoologica Lituanica 13, 37.
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. 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.
Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T. J., Higgins, D. G. and Thompson, J. D. (2003). Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Research 31, 34973500. doi: 10.1093/nar/gkg500.
Deksne, G., Laakkonen, J., Näreaho, A., Jokelainen, P., Holmala, K., Kojola, I. and Sukura, A. (2012). Endoparasites of the Eurasian lynx (Lynx lynx) in Finland. Journal of Parasitology (in Press) doi: 10.1645/GE-3161.1.
Galimberti, A., Romano, D. F., Genchi, M., Paoloni, D., Vercillo, F., Bizzarri, L., Sassera, D., Bandi, C., Genchi, C., Ragni, B. and Casiraghi, M. (2012). Integrative taxonomy at work: DNA barcoding of taeniids harboured by wild and domestic cats. Molecular Ecology Resources 12, 403413.
Haukisalmi, V., Lavikainen, A., Laaksonen, S. and Meri, S. (2011). Taenia arctos n. sp. (Cestoda: Cyclophyllidea: Taeniidae) from its definitive (brown bear Ursus arctos Linnaeus) and intermediate (moose/elk Alces spp.) hosts. Systematic Parasitology 80, 217230. doi: 10.1007/s11230-011-9324-9.
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: origins 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., Galbreath, K. E., Cook, J. A., Kutz, S. J. and Polley, L. (2012). Northern host-parasite assemblages: history and biogeography on the borderlands of episodic climate and environmental transition. Advances in Parasitology 79, 197.
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.
Hüttner, M., Siefert, L., Mackenstedt, U. and Romig, T. (2009). A survey of Echinococcus species in wild carnivores and livestock in East Africa. International Journal for Parasitology 39, 12691276.
Jeon, H. K., Kim, K. H. and Eom, K. S. (2007). Complete sequence of the mitochondrial genome of Taenia saginata: comparison with T. solium and T. asiatica . Parasitology International 56, 243246.
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.
Jia, W. Z., Yan, H. B., Guo, A. J., Zhu, X. Q., Wang, Y. C., Shi, W. G., Chen, H. T., Zhan, F., Zhang, S. H., Fu, B. Q., Littlewood, D. T. and Cai, X. P. (2010). Complete mitochondrial genomes of Taenia multiceps, T. hydatigena and T. pisiformis: additional molecular markers for a tapeworm genus of human and animal health significance. BMC Genomics 11, 447.
Jia, W., Yan, H., Lou, Z., Ni, X., Dyachenko, V., Li, H. and Littlewood, D. T. (2012). Mitochondrial genes and genomes support a cryptic species of tapeworm within Taenia taeniaeformis . Acta Tropica 123, 154163.
Jones, A. and Pybus, M. J. (2001). Taeniasis and echinococcosis. In Parasitic Diseases of Wild Mammals, 2nd Edn (ed. Samuel, W. M., Pybus, M. J. and Kocan, A. A.), pp. 150192. Manson Publishing, London, UK.
Kazlauskas, J., and Matuzevicius, A. (1981). On the helminth fauna and ecology of lynxes in Lithuania. Acta Parasitologica Lituanica 19, 811. (in Russian).
Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111120.
Knapp, J., Nakao, M., Yanagida, T., Okamoto, M., Saarma, U., Lavikainen, A. and Ito, A. (2011). Phylogenetic relationships within Echinococcus and Taenia tapeworms (Cestoda: Taeniidae): an inference from nuclear protein-coding genes. Molecular Phylogenetics and Evolution 61, 628638.
Lavikainen, A., Haukisalmi, V., Lehtinen, M. J., Henttonen, H., Oksanen, A. and Meri, S. (2008). A phylogeny of members of the family Taeniidae based on the mitochondrial cox1 and nad1 gene data. Parasitology 135, 14571467. doi: 10.1017/S003118200800499X.
Lavikainen, A., Haukisalmi, V., Lehtinen, M. J., Laaksonen, S., Holmström, S., Isomursu, M., Oksanen, A. and Meri, S. (2010). Mitochondrial DNA data reveal cryptic species within Taenia krabbei . Parasitology International 59, 290293. doi: 10.1016/j.parint.2010.03.003.
Lavikainen, A., Laaksonen, S., Beckmen, K., Oksanen, A., Isomursu, M. and Meri, S. (2011). Molecular identification of Taenia spp. in wolves (Canis lupus), brown bears (Ursus arctos) and cervids from North Europe and Alaska. Parasitology International 60, 289295. doi: 10.1016/j.parint.2011.04.004.
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.
Liu, G. H., Lin, R. Q., Li, M. W., Liu, W., Liu, Y., Yuan, Z. G., Song, H. Q., Zhao, G. H., Zhang, K. X. and Zhu, X. Q. (2011). The complete mitochondrial genomes of three cestode species of Taenia infecting animals and humans. Molecular Biology Reports 38, 22492256.
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.
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. Journal of Parasitology 89, 633635.
Okamoto, M., Bessho, Y., Kamiya, M., Kurosawa, T. and Horii, T. (1995). 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.
Petrov, A. M. and Potekhina, L. F. (1953). Helminths of carnivores in Tadzhikistan. Trudy Vsesoyuznogo Instituta Gel'mintologii 5, 8294. (In Russian.)
Posada, D. and Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817818.
Pulliainen, E. (1981). Winter diet of Felis lynx L. in SE Finland as compared with nutrition of other northern lynx. Zeitschrift für Säugetierkunde 46, 249259.
Pulliainen, E., Lindgren, E. and Tunkkari, P. S. (1995). Influence of food availability and reproductive status on the diet and body condition of the European lynx in Finland. Acta Theriologica 40, 181196.
Rausch, R. L. (1981). Morphological and biological characteristics of Taenia rileyi Loewen, 1929 (Cestoda: Taeniidae). Canadian Journal of Zoology 59, 653666.
Rossin, M. A., Timi, J. T. and Hoberg, E. P. (2010). An endemic Taenia from South America: validation of T. talicei Dollfus, 1960 (Cestoda: Taeniidae) with characterization of metacestodes and adults. Zootaxa 2636, 4958.
Smith, J. D., Addison, E. M., Joachim, D. G., Smith, L. M. and Quinn, N. W. S. (1986) Helminth parasites of Canada lynx (Felis canadensis) from northern Ontario. Canadian Journal of Zoology 64, 358364.
Shults, L. M. (1982). Taenia wyolagus sp. n. (Cestoda: Taeniidae) from bobcats (Lynx rufus) and cottontail rabbits (Sylvilagus nuttalli): Description, life history and distribution. M.Sc. thesis. University of Wyoming, Laramie, WY, USA.
Swofford, D. L. (2002). PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4 beta Version. Sinauer Associates, Sunderland, MA, USA.
Valdmann, H., Moks, E. and Talvik, H. (2004). Helminth fauna of Eurasian lynx (Lynx lynx) in Estonia. Journal of Wildlife Diseases 40, 356360.
Verster, A. (1969). A taxonomic revision of the genus Taenia Linnaeus, 1758 S.str. Onderstepoort Journal of Veterinary Research 36, 358.
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.
Zyll de Jong, C. G., van, (1966). Parasites of the Canada lynx, Felis (Lynx) canadensis (Kerr). Canadian Journal of Zoology 44, 499509.
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