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Phylogeny and morphology of some European cyathocotylid digeneans (Trematoda: Diplostomoidea)

Published online by Cambridge University Press:  31 May 2024

S.G. Sokolov Open the ORCID record for S.G. Sokolov [Opens in a new window] ,
S.A. Vlasenkov Open the ORCID record for S.A. Vlasenkov [Opens in a new window] ,
S.V. Bugmyrin Open the ORCID record for S.V. Bugmyrin [Opens in a new window] ,
A.P. Kalmykov Open the ORCID record for A.P. Kalmykov [Opens in a new window]  and
D.I. Lebedeva Open the ORCID record for D.I. Lebedeva [Opens in a new window]
S.G. Sokolov
Affiliation:
A.N. Severtsov Institute of Ecology and Evolution, Moscow 119071, Russia
S.A. Vlasenkov
Affiliation:
Institute of Biology, Karelian Research Centre, RAS, Petrozavodsk 185000, Russia
S.V. Bugmyrin
Affiliation:
Institute of Biology, Karelian Research Centre, RAS, Petrozavodsk 185000, Russia
A.P. Kalmykov
Affiliation:
Astrakhan State Natural Biosphere Reserve, Astrakhan 414021, Russia Astrakhan Museum-Reserve, Astrakhan 414000, Russia
D.I. Lebedeva*
Affiliation:
Institute of Biology, Karelian Research Centre, RAS, Petrozavodsk 185000, Russia
*
Corresponding author: D.I. Lebedeva; Email: daryal78@gmail.com
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Abstract

The Cyathocotylidae Mühling, 1898 is a family of primitive diplostomoid trematodes important for understanding the evolution of the superfamily Diplostomoidea. However, cyathocotylids remain poorly studied with the use of molecular techniques. In this study we sequenced the 5.8S + ITS2 region, 28S rRNA, and cox1 genes of two cyathocotylid species and obtained new morphological data on them. We propose Georduboisia nom. nov. instead of the preoccupied name Duboisia Szidat, 1936 (junior homonym of Duboisia Stremme, 1911). Adults of Georduboisia cf. teganuma (Ishii, 1935) and Paracoenogonimus ovatus Katsurada, 1914 were collected from fish-eating birds in the south of the European part of Russia. Georduboisia cf. teganuma was very similar to G. teganuma but differed from it in the shape of the testes. The 28S rRNA gene dataset provided the best-resolved phylogeny of the Cyathocotylidae to date. In the phylogram based on partial sequences of this gene, P. ovatus was close to members of Holostephanoides Dubois, 1983, Neogogatea Chandler & Rausch, 1947 and Gogatea Szidat, 1936. Georduboisia cf. teganuma clustered with members of Cyathocotyle Mühling, 1896 and Holostephanus Szidat, 1936. Phylogenetic analysis based on the 5.8S + ITS2 dataset showed that adults of P. ovatus examined in our study were conspecific with the metacercariae from the musculature of fish collected in Hungary and Italy. It also revealed probable misidentifications of larvae and adults of cyathocotylids whose sequences are deposited in GenBank NCBI.

Keywords

Duboisia teganumaParacoenogonimus ovatusCircus aeruginosusPodiceps cristatusspecies identification
Type
Research Paper
Information
Journal of Helminthology , Volume 98 , 2024 , e44
Copyright
© The Author(s), 2024. Published by Cambridge University Press

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Footnotes

ZooBank publication registration: urn:lsid:zoobank.org:pub:C4C90D05-15C5-4922-9950-2E128A635CCD

References

Achatz, TJ, Pulis, EE, Junker, K, Binh, TT, Snyder, SD, Tkach, VV (2019). Molecular phylogeny of the Cyathocotylidae (Digenea, Diplostomoidea) necessitates systematic changes and reveals a history of host and environment switches. Zoologica Scripta 48, 545–556. doi:10.1111/zsc.12360CrossRefGoogle ScholarPubMed
Achatz, TJ, Martens, JR, Kostadinova, A, Pulis, EE, Orlofske, SA, Bell, JA, Fecchio, A, Oyarzún-Ruiz, P, Syrota, YY, Tkach, VV (2022). Molecular phylogeny of Diplostomum, Tylodelphys, Austrodiplostomum and Paralaria (Digenea: diplostomidae) necessitates systematic changes and reveals a history of evolutionary host switching events. International Journal of Parasitology 52, 47–63. doi:10.1016/j.ijpara.2021.06.002CrossRefGoogle ScholarPubMed
Bayanov, MG, Islamov, MG (1977). On the biology of trematode Duboisia teganuma (Ishii, 1935), a parasite of grebes. In Ershov, VS (ed), Materialy Nauchnoi Conferencii Vsesoyuznogo Obschestva Gel’mintologov, 29. Moscow: Nauka, 6–8.Google Scholar
Besprozvannykh, VV, Ermolenko, AV (2009). Life-cycle of Paracoenogonimus ussuriensis sp. n. (Digenea: Cyathocotylidae) in the Primorsky region (southern Far East, Russia). Helminthologia 46, 100–106. doi:10.2478/s11687-009-0020-0CrossRefGoogle Scholar
Bowles, J, Blair, D, McManus, D (1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology, 54, 165–173. doi:10.1016/0166-6851(92)90109-wCrossRefGoogle ScholarPubMed
Cech, G, Sándor, D, Molnár, K, Varga, Á, Caffara, M, Fioravanti, ML, Buchmann, K, Székely, C (2021). Digenean trematodes in Hungarian freshwater aquacultures. Food and Waterborne Parasitology 22, e00101. doi:10.1016/j.fawpar.2020.e00101CrossRefGoogle ScholarPubMed
Darriba, D, Taboada, GL, Doallo, R, Posada, D (2012). jModeltest2: More models, new heuristics and parallel computing. Nature Methods 9, 772. doi:10.1038/nmeth.2109CrossRefGoogle Scholar
Dorzhiev, TsZ, Badmaeva, EN, Dugarov, ZhN (2021). Helminths in wetland birds of Baikal Siberia: Taxonomic diversity and distribution by hosts. Nature of Inner Asia 1, 23–65. doi:10.18101/2542-0623-2021-1-23-65Google Scholar
Dubois, G (1936). Nouveaux principes de classification des Trématodes du groupe des Strigeida. Revue Suisse de Zoologie 43, 507–515. doi:10.5962/bhl.part.117684CrossRefGoogle Scholar
Dubois, G (1938). Monographie des Strigeida (Trematoda). Mémoires de la Société des Sciences Naturelles de Neuchâtel 6, 1–535.Google Scholar
Dubois, G (1953). Systématique des Strigeida. Complément de la monographie. Mémoires de la Société des Sciences Naturelles de Neuchâtel 8, 1–141.Google Scholar
Dubois, G (1970). Les fondements de la taxonomie des Strigeata La Rue (Trematoda:Strigeida). Revue Suisse de Zoologie 77, 663–685.CrossRefGoogle Scholar
Dubois, G (1983). Les trématodes des genres Prohemistomum Odhner, 1913 et Paracoenogonimus Katsurada, 1914 (Strigeata: Cyathocotyloidea). Annales de parasitologie humaine et comparée 58, 549–556.CrossRefGoogle ScholarPubMed
Dubois, G (1984). Les genres Prosostephanus Lutz, 1935 et Duboisia Szidat, 1936 (Trematoda: Strigeata: Cyathocotyloidea). Revue Suisse de Zoologie 91, 149–155.CrossRefGoogle Scholar
Dubois, G (1987). Systématique des Cyathocotyloidea (Trematoda: Strigeata). Bulletin de la Société des sciences naturelles de Neuchâtel 110, 41–43.Google Scholar
Dubois, G, Beverley-Burton, M (1971). Quelques Strigeata (Trematoda) d’oiseaux de Rhodesie et de Zambie. Bulletin de la Société des sciences naturelles de Neuchâtel 94, 5–19.Google Scholar
Edelényi, B (1974). Mételyek II.—Trematodes II. Közvetett fejlődéstí mételyek—Digenea. Budapest:Akadémiai Kiadó.Google Scholar
Filimonova, LV, Shalyapina, VI (1975). Trematodes of water and marsh birds. In Ryzhikov, KM, Folitarek, SS (eds), Parasites in Natural Complexes of North Kulunda. Novosibirsk: Nauka, Siberian Branch, 35–52.Google Scholar
Ginetsinskaya, TA, Koscheva, AF (1959). On the life cycle and systematic status of Paracoenogonimus ovatus Katsurada (Trematoda) and identity of metacercariae of this species with Neodiplostomum hughes Markewitsh. Vestnik Leningradskogo universiteta, Seria Biologicheskaya 2, 68–75.Google Scholar
Golovin, OV (1958). Helminths of the white-tailed eagle in Kalinin region. Bulletin de la Société impériale des naturalistes de Moscou. Section biologique 1, 93–96.Google Scholar
ICZN (1999). International Code of Zoological Nomenclature. Fourth Edition. London: The International Trust for Zoological Nomenclature.Google Scholar
Ishii, N (1935). Studies on bird trematodes. III. Bird trematodes in Japan. IV. Seven new bird trematodes. Japanese Journal of Experimental Medicine 13, 467–479.Google Scholar
Janchev, J (1958). Untersuchungen über einige Helminthen und Helminthosen bei weissen Störchen und Pelikanen. Izvestia na Zoologicheckiya Institut BAN 7, 393–416.Google Scholar
Komiya, Y (1938). Die Entwicklung des Exkretionssystems einiger Trematodenlarven aus Alster und Elbe, nebst Bemerkungen über ihren Entwicklungszyklus. Zeitschrift fur Parasitenkunde 10, 340–385. doi:10.1007/bf02123446CrossRefGoogle Scholar
Kumar, S, Stecher, G, Li, M, Knyaz, C, Tamura, K (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549. doi:10.1093/molbev/msy096CrossRefGoogle ScholarPubMed
La Rue, GR (1926). Studies on the trematode family Strlgeidae (Holostomidae) No. II. Taxonomy. Transactions of the American Microscopical Society 45, 11–19. doi:10.2307/3221860CrossRefGoogle Scholar
Littlewood, DTJ, Curini-Galletti, M, Herniou, EA. (2000). The interrelationships of proseriata (Platyhelminthes: seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution, 16, 449–466. doi:10.1006/mpev.2000.0802CrossRefGoogle ScholarPubMed
Lutz, A (1935). Observações e considerações sobre Cyathocotylineas e Prohemistomineas. Memórias do Instituto Oswaldo Cruz 30, 157–168. doi:10.1590/S0074-02761935000800002CrossRefGoogle Scholar
Manter, HW (1970). The terminology and occurrence of certain structures of digenetic trematodes, with special reference to the Hemiuroidea. In Singh, KS, Tandan, BK, Srivastava, HD (eds), Commemoration Volume. Izatnagar: Indian Veterinary Research Institute, 27–33.Google Scholar
Mishchenko, VF (1974). Life cycle and ontogenesis of the trematode Linslowiella viviparae (Prohemistomatidae). Trudy GELAN AN SSSR 24, 102–112.Google Scholar
Morgan, JA, Blair, D (1998). Relative merits of nuclear ribosomal internal transcribed spacers and mitochondrial CO1 and ND1 genes for distinguishing among Echinostoma species (Trematoda). Parasitology 116, 289–297. doi:10.1017/S0031182097002217CrossRefGoogle ScholarPubMed
Mühling, P (1896). Beiträge zur Kenntniss der Trematoden. Archiv für Naturgeschichte 62, 243–279.Google Scholar
Mühling, P (1898). Die Helminthen-Fauna der Wirbeltiere Ostpreussens. Archiv für Naturgeschichte 64, 1–118.Google Scholar
Niewiadomska, K (2002). Family Cyathocotylidae Muhling, 1898. In Gibson, DI, Jones, A, Bray, RA (eds), Keys to the Trematoda Vol. 1. Wallingford, UK: CABI Publishing and the Natural History Museum, 201–214. doi:10.1017/S0031182002222830CrossRefGoogle Scholar
Niewiadomska, K (2010). Fauna słodkowodna Polski. 34A. Przywry (Trematoda).Część ogólna; Część systematyczna – Aspidogastrea, Digenea: Strigeida. Łódź: Wydawnictwo Uniwersytetu Łódzkiego.CrossRefGoogle Scholar
Pérez-Ponce de León, G, Hernández-Mena, DI (2019). Testing the higher-level phylogenetic classification of Digenea (Platyhelminthes, Trematoda) based on nuclear rDNA sequences before entering the age of the ‘next-generation’ Tree of Life. Journal of Helminthology 93, 260–276. doi:10.1017/S0022149X19000191CrossRefGoogle ScholarPubMed
Odening, K (1963). Strigeida aus Vögeln des Berliner Tierparks. Angew. Parasiotologie 4, 171–242.Google Scholar
Ostrowska, K, Wiśniewski, G, Piasecki, W (2019). Spatial distribution of skin and muscle metacercariae (Digenea) of roach, Rutilus rutilus, and bleak, Alburnus alburnus (Actinopterygii: Cypriniformes: Cyprinidae), from an estuary lake in central Europe. Acta Ichthyologica et Piscatoria 49, 421–429. doi:10.3750/AIEP/02823CrossRefGoogle Scholar
Poche, F (1925). Das System der Platodaria. Archiv für Naturgeschichte. Abteilung A 91: 1–458.Google Scholar
Rambaut, A (2012). FigTree v1. 4. Molecular evolution, phylogenetics and epidemiology. Available at: https://github.com/rambaut/figtree/releases (accessed 1 January 2024).Google Scholar
Ronquist, F, Teslenko, M, Van Der Mark, P, Ayres, DL, Darling, A, Höhna, S, Huelsenbeck, JP (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542. doi:10.1093/sysbio/sys029CrossRefGoogle ScholarPubMed
Sándor, D, Gyöngy, M, Nyeste, K, Czeglédi, I, Székely, C, Buchmann, K, Cech, G (2020). Digenean Holostephanus (Trematoda: Digenea: Cyathocotylidae) metacercariae in common carp (Cyprinus carpio Linnaeus, 1758) muscle: Zoonotic potential and sensitivity to physico-chemical treatments. Journal of Helminthology 94, e117. doi:10.1017/S0022149X1900110XCrossRefGoogle ScholarPubMed
Sokolov, SG, Khrustalev, AV, Greenwood, SJ, Gray, CN, Robbins, WT, Jones, MEB, Voropaeva, EL, Kalmykov, AP, Dzhamirzoev, GS, Atopkin, DM (2023). Phylogenetic assessment of apophallines (Digenea: Opisthorchiidae) with revision of Apophallus donicus Skrjabin & Lindtrop, 1919 complex and some taxonomic propositions. Systematic and Biodiversity 21, 2189898. doi:10.1080/14772000.2023.2189898CrossRefGoogle Scholar
Sudarikov, VE (1961). Order Strigeidida (La Rue, 1926) Sudarikov, 1959. Part 4. Suborder Cyathocotylata Sudarikov, 1959. In Skrjabin, KI (ed), Osnovy Trematodologii . Vol. 19. Moscow: Izdatel’stvo Akademii Nauk SSSR, 268–469.Google Scholar
Sudarikov, VE, Shigin, AA, Zhatkanbaeva, AD (1973). The trematode Cyathocotyle teguana Ishii, 1935 and its taxonomic status. Parazitologiya 7, 58–60.Google Scholar
Stremme, H (1911). Die Säugetiere mit Ausnahme der Proboscidier. In SELENKA, L, BLANCKENHORN, M (eds), Die Pithecanthropus-Schichten auf Java. Leipzig: Engelmann, 82–150.Google Scholar
Szidat, L (1936). Parasiten aus Seeschwalben. I. Über neue Cyathocotyliden aus dem Darm von Sterna hirundo L. und Sterna paradisea. Zeitschrift fur Parasitenkunde 8, 285–316. doi:10.1007/BF02122314CrossRefGoogle Scholar
Tkach, VV, Littlewood, DTJ, Olson, PD, Kinsella, JM, Swiderski, Z (2003). Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56, 1–15. doi:10.1023/A:1025546001611CrossRefGoogle ScholarPubMed
Tkach, V, Pawlowski, J, Mariaux, J (2000). Phylogenetic analysis of the suborder plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. International Journal of Parasitology 30, 83–93. doi:10.1016/s0020-7519(99)00163-0CrossRefGoogle ScholarPubMed
Wierzbicka, J, Einszporn-Orecka, T (1972). Metacercariae of Paracoenogonimus ovatus as a causativeagent of emaciation of common bream. Gospodarka Rybna 8, 4–7.Google Scholar
Yamaguti, S (1971). Synopsis of digenetic trematodes of vertebrates. Vol. 1. Tokyo: Keigaku Publishing.Google Scholar
Zhatkanbaeva, D (1964). Helminth fauna of waterbirds in the Kazakh SSR. Trudy Instituta Zoologii i Parazitologii Akademii Nauk Kazakhskoi SSR 22, 110–125.Google Scholar
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