Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter July 5, 2017

The systematic position and structure of the genus Leyogonimus Ginetsinskaya, 1948 (Platyhelminthes: Digenea) with comments on the taxonomy of the superfamily Microphalloidea Ward, 1901

Gerard Kanarek, Grzegorz Zaleśny, Jiljí Sitko and Vasyl V. Tkach
From the journal Acta Parasitologica

Abstract

The systematic position, phylogenetic relationships and composition of the genus Leyogonimus Ginetsinskaya, 1948 have always been uncertain. In the present study, we investigate the taxonomic position and phylogenetic relationships between the type-species L. polyoon (Linstow, 1887) and L. postgonoporus (Neiland, 1951) (previously classified as Macyella), based on newly obtained partial sequences of the nuclear large ribosomal subunit DNA. To test some of the previously proposed systematic arrangements, we have also sequenced specimens of Stomylotrema vicarium Braun, 1901 and Phaneropsolus sp. Our results clearly demonstrate that both L. polyoon and L. postgonoporus belong to the family Pleurogenidae Looss, 1899 within the superfamily Microphalloidea. Thus, the Leyogonimidae Dollfus, 1951 should be recognized as a synonym of the Pleurogenidae. Leyogonimus polyoon clearly constitutes a separate, sister branch to the clade consisting of Collyricloides massanaeVaucher, 1969 and L. postgonoporus. Based on these results, we resurrect the genus MacyellaNeiland, 1951 with type-species M. postgonoporus. Besides, Collyricloides Vaucher, 1968 is synonymized with Macyella resulting in new combination Macyella massanae (Vaucher, 1968) comb. nov. Molecular phylogenetic analysis has demonstrated the lack of a close phylogenetic relationships between Stomylotema vicarium and Leyogonimus previously placed by several authors into the family Stomylotrematidae Poche, 1925. The status of the Phaneropsolidae Mehra, 1935 as independent family was confirmed with the addition of the newly sequenced Phaneropsolus sp. from China.

Acknowledgments

We thank Eric Pulis (Institute for Marine Mammal Studies, Gulfport, Mississippi, USA) for his useful comments on the draft of the manuscript, Kaylyn Patitucci (Univerity of North Dakota) for collecting Stomylotrema vicarium in the field and help with its laboratory processing, and Sara Bush (University of Utah, Salt Lake City, USA) for providing frozen intestine of Indian Paradise Flycatcher that yielded specimens of Phaneropsolus sp. This study was partly supported by the Polish Ministry of Science and Higher Education grant IP2010 016570 for GK and the grant DEB 1120734 from the National Science Foundation (USA) to VVT.

References

Braun M. 1902. Fascioliden der Vögel. Zoologische Jahrbücher. Abtheilung für Systematik, Geographie un Biologie der Thiere, 16, 1–162. (In German)Search in Google Scholar

Coil W.H., Kuntz R.E. 1958. Records of trematodes collected in Turkey with the descriptions of new species in the families Lecithodendriidae and Plagiorchiidae. Proceedings of the Helminthological Society of Washington, 25, 61–67Search in Google Scholar

Dollfus R-P. 1951. Sur “Distomum polyoon” O. von Linstow, parasite mal connu du Ralliforme Gallinula chloropus (L.). Annales de Parasitologie Humaine et Comparée, 26, 128–131. (In French)10.1051/parasite/1951261128Search in Google Scholar

Filimonova L.V. 1973. Lobogonimus skrjabini gen. nov. sp. nov. – a new trematode from red-necked grebe In: (Ed. V.G. Gagarin) Problems of general and applied helminthology, Moscov, Izdaliel’stvo Nauka, 155–157Search in Google Scholar

Groschaft J. 1969. First finding of the trematode Macyella postgonoporus Neiland, 1951 in Europe. Folia Parasitologica, 16, 265–269Search in Google Scholar

Heneberg P., Literák I. 2013. Molecular phylogenetic characterization of Collyriclum faba with reference to its three host-specific ecotypes. Parasitology International, 62, 262–267. 10.1016/j.parint.2013.01.002Search in Google Scholar

Huelsenbeck J.P., Ronquist F. 2001. MrBayes: Bayesian inference of phylogeny. Bioinformatics, 17, 754–755. 10.1093/bioinformatics/17.8.754Search in Google Scholar

Jancev J.I. 1974. Macyella vassilevi n. sp. (Lecithodendriidae) from Apodemus sylvaticus in Bulgaria. Comptes rendus de l’Académie bulgare des Sciences, 27, 89–92Search in Google Scholar

Jourdane J., Triquell, A. 1973. Digènes parasites d’Apodemus sylvaticus (L.) dans la partie orientale des Pyrénées. Description de Macyella apodemi sp. n. Bulletin du Museum Nationale d’Histoire Naturelle, 117, 351–361. (In French)Search in Google Scholar

Kanarek G., Zaleśny G., Czujkowska A., Sitko J., Harris P.D. 2015. On the systematic position of Collyricloides massanae Vaucher, 1969 (Platyhelminthes: Digenea) with notes on distribution of this trematode species. Parasitology Research, 114, 1495–1601. 10.1007/s00436-015-4333-2Search in Google Scholar

Kanarek G., Zaleśny G., Sitko J., Tkach V. 2014. Phylogenetic relationships and systematic position of the families Cortrematidae and Phaneropsolidae (Platyhelminthes: Digenea). Folia Parasitologica, 61, 523–528. 10.14411/fp.2014.057Search in Google Scholar

Khotenovskii I.A. 1971. Addendum to the family Stomylotrematidae Poche, 1926 In: (Ed. K.I. Skryabin) Trematodes of animals and man. Vol. XXIV. Moscov, Izdaliel’stvo Nauka, 357–378Search in Google Scholar

von Linstow O. 1887. Helminthologische Untersuchungen. Zoologische Jahrbücher. Abtheilung für Systematik, Geographie und Biologie der Tiere, 3, 97–114. (In German)Search in Google Scholar

Lotz J.M., Font W.F. 2008. Family Leyogonimidae Dollfus, 1951. In: (Eds. R.D. Bray, D.I. Gibson, A. Jones) Keys to the Trematoda. Vol. III. Wallingford, CAB International and Natural History Museum, 537–54010.1079/9780851995885.0537Search in Google Scholar

Montoliu I., Feliu C. 1986. Macyella apodemi Jourdane et Triquell, 1973 (Trematoda: Lecithodendriidae), parásito intestinal de Eliomys quercinus Linnaeus, 1766 (Rodentia: Gliridae) en el Pirineo catalán. Circular Farmaceutica, 290, 11–16. (In Spanish)Search in Google Scholar

Neiland K.A. 1951. A new genus of trematode (Lecithodendriidae: Pleurogenetinae) from varied thrush. Journal of Parasitology, 37, 563–56810.2307/3273349Search in Google Scholar

Odening K. 1959. Das Exkretionssytem von Omphalometra und Brachycoelium (Trematoda, Digenea) und die Taxonomie der Unterordnung Plagiorchiata. Parasitology Research, 19, 442–457. (In German)10.1007/BF00259735Search in Google Scholar

Odening K. 1964. Dicrocoelioidea und Microphalloidea (Trematoda: Plagiorchiata) aus Vögeln des Berliner Tierparks. Mitteilungen aus dem Zoologischen Museum in Berlin, 40, 145–184. (In German)10.1002/mmnz.4830400205Search in Google Scholar

Okulewicz J., Wesołowska M. 2003. Rediscovery of Leyogonimus postgonoporus (Neiland, 1951) (Trematoda, Stomylotrematidae) in Central Europe. Acta Parasitologica, 48, 233–236Search in Google Scholar

Olson P.D., Cribb T.H., Tkach V., Bray R.A., Littlewood D.T.J. 2003. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology, 33, 733–755. 10.1016/S0020-7519(03)00049-3Search in Google Scholar

Ribas A., Casanova J.C., Miquel J., Fons R., Giusset C., Feliu C. 2005. On the fauna of digenetic trematodes, parasites of small mammals, in the Natural Reserves of Py and Mantet (Oriental Pyrenees, France). Helminthologia, 42, 71–75Search in Google Scholar

Schwarz J. 1981. Über den Lebenszyklus des Trematoden Collyricloides massanae Vaucher 1969 (Trematoda: Collyrididae) und seine Entwicklungsstadien. Beiträge zur Naturkunde in Osthessen, 17, 85–99. (In German)Search in Google Scholar

Sharpilo V.P., Iskova N.I.(Eds) 1989. The Fauna of the Ukraine. Trematoda: Plagiorchiata. Naukova Dumka, KievSearch in Google Scholar

Skarbilovitch T.S. 1948. Family Lecithodendriidae Odhner, 1911. In: (Ed. K.I. Skryabin) Trematodes of animals and man. Vol. II. Moscov, Izdatel’stvo Akademii Nauk SSSR, 337–690Search in Google Scholar

Tkach V., Pawlowski J. 1999. A new method of DNA extraction from the ethanol-fixed parasitic worms. Acta Parasitologica, 44, 147–148Search in Google Scholar

Tkach V., Pawlowski J., Mariaux J. 2000. Phylogenetic analysis of the suborder Plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. International Journal for Parasitology, 30, 83–93. 10.1016/S0020-7519(99)00163-0Search in Google Scholar

Tkach V.V., Pawlowski J., Mariaux J., Świderski Z. 2001. Molecular phylogeny of the suborder Plagiorchiata and its position in the system of Digenea. In: (Eds D.T.J Littlewood, R.A. Bray) Interrelationships of the Platyhelminthes. London, Taylor & Francis, 186–193Search in Google Scholar

Tkach V.V., Littlewood D.T.J., Olson P.D., Kinsella J.M., Świderski Z. 2003. Molecular phylogenetic analysis of the Microphalloidea Ward, 1901. Systematic Parasitology, 56, 1–15. 10.1023/A:1025546001611Search in Google Scholar

Vaucher C. 1969. Collyricloides massanae n. gen. n. sp. (Collyriclidae) trematode vivant dans kystes de l’intestin du mulot Apodemus flavicollis (Melchior). Vie et Milieu, 20, 29–39. (In French)Search in Google Scholar

Yamaguti S.(Ed.) 1958. Systema Helminthum. Volume I. The Digenetic trematodes of vertebrates. Interscience Publishers Inc., New YorkSearch in Google Scholar

Yamaguti S. (Ed.) 1971. Synopsis of Digenetic Trematodes of Vertebrates. Vol. I. Keigaku Publishing, TokyoSearch in Google Scholar

Received: 2017-3-17
Revised: 2017-5-2
Accepted: 2017-5-5
Published Online: 2017-7-5
Published in Print: 2017-9-26

© 2017 W. Stefański Institute of Parasitology, PAS