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Published: 2010-05-31
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Taxonomic review of cestodes of the genus Catenotaenia Janicki, 1904 in Eurasia and molecular phylogeny of the Catenotaeniidae (Cyclophyllidea)

Finnish Forest Research Institute, Vantaa Research Unit, PO Box 18, 01301 Vantaa, Finland
Finnish Forest Research Institute, Vantaa Research Unit, PO Box 18, 01301 Vantaa, Finland
Finnish Forest Research Institute, Vantaa Research Unit, PO Box 18, 01301 Vantaa, Finland
Platyhelminthes Parasites tapeworms Cestoda 28S rRNA Skrjabinotaenia Meggittina Catenotaenioides n. g. Catenotaenia apodemi n. sp. Catenotaenia cricetuli n. sp. Catenotaenia microti n. sp. rodents

Abstract

This study reviews the taxonomy of cestodes of the genus Catenotaenia Janicki, 1904 (Cyclophyllidea: Catenotaeniidae) in Eurasia and presents the first molecular phylogenetic hypothesis of Catenotaenia, Skrjabinotaenia Ahumyan, 1946 and Meggittina Lynsdale, 1953, all parasites of rodents. The phylogenetic data are based on sequences of 28S ribosomal RNA. The analysis does not support the proposed subfamilial classification of the Catenotaeniidae into Catenotaeniinae Spasskii, 1949 and Skrjabinotaeniinae Genov & Tenora, 1979. Instead, the main division appears to be between Eurasian species and a basal Nearctic species. The results support the monophyly of the Skrjabinotaeniinae but not that of the Catenotaeniinae or Catenotaenia as traditionally understood. It is suggested that the Old World catenotaeniid cestodes appeared in murid rodents and diverged subsequently as Skrjabinotaenia and Meggittina (Skrjabinotaeniinae) in Africa. According to the molecular phylogeny, Eurasian Catenotaenia codiverged with their hosts, with the exception of Catenotaenia dendritica that originated via a host shift from murid rodents to squirrels. The crown clade of Eurasian Catenotaenia consists only of species found in cricetid rodents and the three terminal species only in the Arvicolinae (voles). Phylogenetic structure within the Eurasian Catenotaenia clade suggests seven distinct lineages, three of which are described as new: C. apodemi n. sp. from Apodemus peninsulae (type host) from the Republic of Buryatia and from Apodemus uralensis from the Lower Tunguska River, North-Central Siberia (Russian Federation); C. cricetuli n. sp. from Cricetulus barabensis from the Republic of Buryatia and C. microti n. sp. from Microtus socialis from Kazakhstan. A new genus (Catenotaenioides n. g.) is proposed for C. kirgizica Tokobaev, 1959, a basal species within the Old World clade. Of the various morphological features, proglottid form (short acraspedote proglottids widest at middle vs. elongated craspedote proglottids widest posteriorly) is consistent with the phylogenetic pattern exhibited by catenotaeniid cestodes.

References

  1. Abramson, N.I., Rodchenkova, E.N. & Kostygov, A.Y. (2009) Genetic variation and phylogeography of the bank vole (Clethrionomys glareolus, Arvicolinae, Rodentia) in Russia with special reference to the introgression of the mtDNA of a closely related species, red-backed vole (Cl. rutilus). Russian Journal of Genetics, 45, 533–545.

    Ahumyan, K.S. (1946) K perestorojke sistematiki cestod roda Catenotaenia Janicki, 1904. In: Gel’mintolog. Sbornik, 40. Let. Deiatelnost K. I. Skrjabin. Izd. Akad. Nauk. SSSR37–41.

    Asakawa, M., Tenora, F., Kamiya, M., Harada, M. & Borkovcova, M. (1992) Taxonomical study of the genus Catenotaenia Janicki, 1904 (Cestoda) from voles in Japan. Bulletin of the Biogeographical Society of Japan, 47, 73–76.

    Babero, B.B. & Cattan, P.E. (1983) Catenotaenia neotomae sp. n. (Cestoda: Dilepidae) parásito de Neotoma lepida (Rodentia: Cricetidae) en Nevada, U.S.A. Boletin Chileno de Parasitologia, 38, 12–16.

    Baer, J.G. (1925) Sur quelques Cestodes du Congo Belge. Revue Suisse de Zoologie, 18, 239–251.

    Bajer, A., Behnke, J.M., Pawelczyk, A., Kulis, K., Sereda, M.J. & Sinski, E. (2005) Medium-term temporal stability of the helminth component community structure in bank voles (Clethrionomys glareolus) from the Mazury Lake District region of Poland. Parasitology, 130, 213–228.

    Conroy, C.J. & Cook, J.A. (1999) MtDNA evidence for repeated pulses of speciation within arvicoline and murid rodents. Journal of Mammalian Evolution, 6, 221–245.

    Cook, J.A., Runck, A.M. & Conroy, C.J. (2004) Historical biogeography at the crossroads of the northern continents: molecular phylogenetics of red-backed voles (Rodentia: Arvicolinae). Molecular Phylogenetics and Evolution, 30, 767–777.

    Dowell, A.M. (1953) Catenotaenia californica, sp. nov., a cestode of the kangaroo rat, Dipodomys panamintinus mohavensis. American Midland Naturalist, 49, 738–742.

    Drummond, A.J., Ashton, B., Cheung, M., Heled, J., Kearse, M., Moir, R., Stones-Havas, S., Thierer, T. & Wilson, A.C. (2009) Geneious v 4.8. Available from http://www.geneious.com/.

    Dujardin, F. (1845) Histoire naturelle des helminthes ou vers intestinaux. De L'Imprimerie de Crapelet, Paris, 654 pp.

    Galewski, T., Tilak, M., Sanchez, S., Chevret, P., Paradis, E. & Douzery, E.J.P. (2006) The evolutionary radiation of Arvicolinae rodents (voles and lemmings): relative contribution of nuclear and mitochondrial DNA phylogenies. BMC Evolutionary Biology, 6, 80.

    Ganzorig, S., Tenora, F. & Kamiya, M. (1999) New records of catenotaeniid cestodes from rodents in Mongolia, with notes on the taxonomy of the Catenotaenia Janicki, 1904 and Hemicatenotaenia Tenora, 1977 (Cestoda: Catenotaeniidae). Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis, 47, 33–38.

    Genov, T. (1984) Helminti na nasekomoyadnite bozajnici i grizachite v Bulgariya (Helminths of insectivorous mammals and rodents in Bulgaria). Izdatelstvo na Bulgarskata Akademiya na Naukite, Sofia, 348 pp.

    Gibson, D.I., Bray, R.A. & Harris, E.A. (2005) Host-Parasite database of the Natural History Museum, London. Available from http://www.nhm.ac.uk/research-curation/research/projects/host-parasites/database/.

    Goeze, J.A.E. (1782) Versuch einer Naturgeschichte der Eingeweidewürmer thierischer Körper. Blankenburg, 471 pp.

    Haukisalmi, V. & Henttonen, H. (1990) The impact of climatic factors and host density on the long-term population dynamics of vole helminths. Oecologia, 83, 309–315.

    Haukisalmi, V. & Henttonen, H. (1993a) Coexistence in helminths of the bank vole Clethrionomys glareolus. I. Patterns of co-occurrence. Journal of Animal Ecology, 62, 221–229.

    Haukisalmi, V. & Henttonen, H. (1993b) Coexistence in helminths of the bank vole Clethrionomys glareolus. II. Intestinal distributions and interspecific interactions. Journal of Animal Ecology, 62, 230–238.

    Haukisalmi, V. & Henttonen, H. (2000) Variability of helminth assemblages and populations in the bank vole Clethrionomys glareolus. Polish Journal of Ecology (Supplement), 48, 219–231.

    Haukisalmi, V., Henttonen, H., Hardman, L.M., Hardman, M., Laakkonen, J., Murueva, G., Niemimaa, J., Shulunov, S. & Vapalahti, O. (2009) Review of tapeworms of rodents in the Republic of Buryatia, with emphasis on anoplocephalid cestodes. ZooKeys, 8, 1–18.

    Haukisalmi, V. & Tenora, F. (1993) Catenotaenia henttoneni sp. n. (Cestoda: Catenotaeniidae), a parasite of voles Clethrionomys glareolus and C. rutilus (Rodentia). Folia Parasitologica, 40, 29–33.

    Huelsenbeck, J.P., Ronquist, F., Nielsen, R. & Bollback, J.P. (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science, 294, 2310–2314.

    Janicki, C. (1904) Zur Kenntnis einiger Säugetiercestoden. Zoologischer Anzeiger, 27, 770–782.

    Janicki, C. (1906) Studien an Säugetiercestoden. Zeitschrift für Wissenschaftliche Zoologie, 81, 505–597.

    Joyeux, C. & Baer, J.G. (1945) Morphologie, évolution et position systématique de Catenotaenia pusilla (Goeze, 1782) Cestode parasite de Rongeurs. Revue Suisse de Zoologie, 52, 13–51.

    Kirshenblat, Y.D. (1949) K gel'mintofaune Zakavkazskogo homyaka (Mesocricetus auratus brandti Nehr.). Uchenye Zapiski Leningradskogo Gosudarstvennogo Universiteta, 101, 111–127.

    Littlewood, D.T., Curini-Galletti, M. & Herniou, E.A. (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution, 16, 449–466.

    Lockyer, A.E., Olson, P.D. & Littlewood, D.T.J. (2003) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biological Journal of the Linnean Society, 78, 155–171.

    Lynsdale, J.A. (1953) On a new remarkable cestode, Meggittina baeri gen. et sp. n. (Anoplocephalinae) from rodents in Southern Rhodesia. Journal of Helminthology, 27, 129–142.

    Maddison, D.R. & Maddison, W.P. (2000) MacClade 4: Analysis of phylogeny and character evolution, version 4.0. Sinauer Associates, Sunderland, MA,pp.

    McIntosh, A. (1941) A new dilepidid cestode, Catenotaenia linsdalei, from a pocket gopher in California. Proceedings of the Helminthological Society of Washington, 8, 60–62.

    Milazzo, C., Casanova, J.C., Aloise, G., Ribas, A. & Cagnin, M. (2003) Helminths of the bank vole Clethrionomys glareolus (Rodentia, Arvicolinae) in Southern Italy. Italian Journal of Zoology, 70, 333–337.

    Musser, G.G. & Carleton, M.D. (2005) Superfamily Muroidea. In: Wilson, D.E. & Reeder, D.M. (Eds), Mammal species of the world. A taxonomic and geographic reference (3rd ed). Johns Hopkins University Press, Baltimore, pp. 894–1531.

    Olson, P.D., Littlewood, D.T., Bray, R.A. & Mariaux, J. (2001) Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Molecular Phylogenetics and Evolution, 19, 443–467.

    Osipova, O.V. & Soktin, A.A. (2008) Experimental simulation of ancient hybridization between bank and red voles. Doklady Biological Sciences, 420, 169–171.

    Posada, D. & Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics, 14, 817–818.

    Quentin, J.-C. (1971) Cestodes Skrjabinotaenia de Rongeurs Muridés et Dendromuridés de Centrafrique. Hypothèse sur l'évolution des Cestodes Catenotaeniinae. Cahiers de La Maboké, 9, 57–79.

    Quentin, J.C. (1994) Family Catenotaeniidae Spasskii, 1950. In: Khalil, L.F., Jones, A. & Bray, R.A. (Eds), Keys to the Cestode Parasites of Vertebrates. CAB International, Cambridge, pp. 367–374.

    Rausch, R. (1951) Studies on the helminth fauna of Alaska. VII - On some helminths from Arctic marmots with the description of Catenotaenia reggiae n. sp. (Cestoda: Anoplocephalidae). Journal of Parasitology, 37, 415–418.

    Riggenbach, E. (1895) Taenia dendritica Goeze. Zentralblatt für Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene. 1. Abt., 17, 710–716.

    Robovský, J., Řičanková, V. & Zrzavý, J. (2008) Phylogeny of Arvicolinae (Mammalia, Cricetidae): utility of morphological and molecular data sets in a recently radiating clade. Zoologica Scripta, 37, 571–590.

    Ronquist, F. & Huelsenbeck, J.P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.

    Rudolphi, C.A. (1819) Entozoorum synopsis cui accedunt mantissa duplex et indices locupletissimi. Augustus Rücker, Berolini, 811 pp.

    Ryzhikov, K.M., Gvozdev, E.V., Tokobaev, M.M., Shaldybin, L.S., Macaberidze, G.V., Merkusheva, I.V., Nadtochii, E.V., Hohlova, I.G. & Sharpilo, L.D. (1978) Opredelitel' gelmintov gryzunov fauny SSSR. Cestody i trematody. Nauka, Moskva, 231 pp.

    Shaykenov, B. (1981) Gel'minty gryzunov Kazahstana. Izdatel'stvo "Nauka" Kazahskoj SSR, Alma-Ata, 172 pp.

    Shimalov, V.V. & Shimalov, V.T. (2002) Helminth fauna of the red squirrel (Sciurus vulgaris Linnaeus, 1758) in Belorussian Polesie. Parasitology Research, 88, 1008.

    Shulz, R.S. & Landa, D.M. (1934) Paraziticheskie chervi bol'choj peschanki (Rhombomys opimus Richt.). Vesti Mikrobiol. Epidemiol. Parasitol., 13, 305–315.

    Smith, C.F. (1954) Four new species of cestodes of rodents from the High Plains, Central and Southern Rockies and notes on Catenotaenia dendritica. Journal of Parasitology, 40, 245–254.

    Spasskii, A.A. (1951) Anoplocephalate tapeworms of domestic and wild animals. Skrjabin, K. I. (Ed), Essentials of cestodology, volume 1. The Academy of Sciences of the USSR, Moscow. Translated from Russian for the U.S. National Science Foundation and Department of Agriculture by the Israel Program for Scientific Translations, 1961. Office of Technical Services, U.S. Department of Commerce, Washington, 783 pp.

    Tegelström, H. (1987) Transfer of mitochondrial DNA from the northern red-backed vole (Clethrionomys rutilus) to the bank vole (C. glareolus). Journal of Molecular Evolution, 24, 218–227.

    Tenora, F. (1959) Reviziya klassifikacii lentochnyh chervej semejstva Catenotaeniidae Sapssky, 1950. Zoologicheskij Zhurnal, 38, 1322–1334.

    Tenora, F. (1964) On the systematic situation of tapeworms of the family Catenotaeniidae Spassky, 1950. Zoologické Listy, 13, 333–352.

    Tenora, F. (1977) Reorganization of the system of cestodes of the genus Catenotaenia Janicki, 1904. Evolutionary implications. Acta Universitatis Agriculturae, Brno, 25, 163–170.

    Tenora, F., Hönigova, M. & Asakawa, M. (1992) Systematic and taxonomical statut [sic] of Catenotaenia Janicki, 1904, (Cestoda). Acta Universitatis Agriculturae, Brno, 40, 221–228.

    Tenora, F., Mas-Coma, S., Murai, É. & Feliu, C. (1980) The system of cestodes of the suborder Catenotaeniata Spassky, 1963. Parasitologica Hungarica, 13, 39–57.

    Tenora, F. & Murai, É. (1975) Cestodes recovered from rodents (Rodentia) in Mongolia. Annales Historico-Naturales Musei Nationalis Hungarici, 67, 65–70.

    Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleid Acid Research, 24, 4876–4882.

    Tokobaev, M.M. (1959) Gel'mintofauna gryzunov Kirgizii. Trudy Inst. Zool. Parasitol. AN KirgSSR, 7, 133–142.

    Wickström, L.M., Haukisalmi, V., Varis, S., Hantula, J. & Henttonen, H. (2005) Molecular phylogeny and systematics of anoplocephaline cestodes in rodents and lagomorphs. Systematic Parasitology, 62, 83–99.

    Yamaguti, S. (1942) Studies on the helminth fauna of Japan. Part 42. Cestodes of mammals, II. Published by the author, Kyoto, 18 pp.