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Molecular and morphological screening of Podocotyle spp. (Trematoda: Opecoelidae) sheds light on their diversity in Northwest Pacific and eastern European Arctic

Published online by Cambridge University Press:  19 October 2023

S. Sokolov Open the ORCID record for S. Sokolov [Opens in a new window] ,
S. Shchenkov Open the ORCID record for S. Shchenkov [Opens in a new window] ,
E. Frolov Open the ORCID record for E. Frolov [Opens in a new window] ,
S. Denisova Open the ORCID record for S. Denisova [Opens in a new window]  and
I. Gordeev Open the ORCID record for I. Gordeev [Opens in a new window]
S. Sokolov
Affiliation:
A.N. Severtsov Institute of Ecology and Evolution, RAS, 119071, Moscow, Russia
S. Shchenkov
Affiliation:
Department of Invertebrate Zoology, St. Petersburg State University, 199034 St. Petersburg, Russia
E. Frolov
Affiliation:
Sakhalin Branch of Russian Federal Research Institute of Fisheries and Oceanography, 693023 Yuzhno-Sakhalinsk, Russia
S. Denisova
Affiliation:
Department of Invertebrate Zoology, St. Petersburg State University, 199034 St. Petersburg, Russia
I. Gordeev*
Affiliation:
Russian Federal Research Institute of Fisheries and Oceanography, 105187 Moscow, Russia Department of Invertebrate Zoology, Lomonosov Moscow State University, 119234 Moscow, Russia
*
Corresponding author: Ilya Gordeev; Email: gordeev_ilya@bk.ru
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Abstract

Podocotyle is a genus of marine opecoelid digeneans that parasitize a wide variety of fish as adults. We present the first phylogenetic analysis of several Podocotyle isolates using nuclear 28S rDNA and mitochondrial cox1 DNA regions. New sequences were obtained for Podocotyle specimens from fish caught in the Sea of Okhotsk and the White Sea. Based on morphological and molecular data, eight Podocotyle lineages of species rank were revealed. However, this diversity is poorly formalized within the current taxonomic model of the genus. As a result, we identified Podocotyle cf. angulata, Podocotyle cf. atomon, Podocotyle cf. reflexa, Podocotyle atomon of Sokolov et al., 2019, Podocotyle sp. of Denisova et al., 2023, Podocotyle sp. 1, Podocotyle sp. 2 and Podocotyle sp. 3. We also highlight the unresolved question of the life cycles of representatives of Podocotyle whose intramolluscan stages parasitize the intertidal snails Littorina spp.

Keywords

Podocotyle angulataPodocotyle apodichthysiPodocotyle atomonPodocotyle reflexaWhite SeaSea of Okhotskcox1 mtDNA28S rDNA
Type
Research Paper
Information
Journal of Helminthology , Volume 97 , 2023 , e78
Copyright
© The Author(s), 2023. Published by Cambridge University Press

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References

Blend, CK and Dronen, NO (2015) Description of a new species of Podocotyle Dujardin, 1845 (Digenea: Opecoelidae: Plagioporinae) from the cusk-eel, Luciobrotula corethromycter Cohen, 1964 (Ophidiiformes: Ophidiidae), from the Gulf of Mexico and Caribbean Sea. Acta Parasitologica 60(2), 234–243.CrossRefGoogle ScholarPubMed
Blend, CK, Dronen, NO and Armstrong, HW (2016) Podocotyle nimoyi n. sp. (Digenea: Opecoelidae: Plagioporinae) and a re-description of Podocotyle pearsei Manter, 1934 from five species of deep-sea macrourids from the Gulf of Mexico and Caribbean Sea. Zootaxa 4117(4), 491–512.Google Scholar
Blend, CK, Dronen, NO and Armstrong, HW (2019) Occurrence of Podocotyle Dujardin, 1845 (Opecoelidae, Podocotylinae) in three species of deep-sea macrourids from the Gulf of Mexico and Caribbean Sea with an updated key to species and host-parasite checklist. Zootaxa 4638(4), 507–533.CrossRefGoogle ScholarPubMed
Bowles, J, Blair, D and McManus, DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54(2) 165–173.CrossRefGoogle ScholarPubMed
Bray, RA and Campbell, RA (1996) New plagioporines (Digenea: Opecoelidae) from deep-sea fishes of the North Atlantic Ocean. Systematic Parasitology 33, 101–113.CrossRefGoogle Scholar
Chubrik, GK (1966) Fauna and ecology of larval trematodes in mollusks of Barents and White Seas. pp. 78–158. In YuI, Polanski (Ed) Life Cycles of Parasitic Worms of North Seas. Moscow, Leningrad, Nauka. [In Russian]Google Scholar
Creplin, FCH (1825) Observationes de entozois. 86 pp. Gryphiswaldiae,: Sumtibus Mauritii Librariipp.Google Scholar
Cribb, TH (2005) Family Opecoelidae Ozaki, 1925. pp. 443–531. In Jones, A, Bray, RA and Gibson, DI (Eds) Keys to the Trematoda 2. Wallingford, CABI Publishing and the Natural History Museum.CrossRefGoogle Scholar
Denisova, SA, Shunatova, NN, Lebedenkov, VV and Shchenkov, SV (2023) Ultrastructure of an opecoelid daughter sporocyst, Podocotyle sp. (Digenea: Opecoelidae): comparative analysis of the somatic tissues and new insights into the organization of the nervous system. Canadian Journal of Zoology 101(7), 579–602.Google Scholar
Dollfus, R.-Ph (1968) Les trématodes de l’histoire naturelle des helminthes de Félix Dujardin (1845). Mémoires du Muséum National d’Histoire Naturelle , Series A 54, 118–196. [In French]Google Scholar
Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.CrossRefGoogle ScholarPubMed
Edmiston, PC (1971). Taxonomic studies on the genus Podocotyle (Trematoda: Opecoelidae). 115 pp. MS thesis, University of the Pacific, California.Google Scholar
Gibson, DJ ( 1974) Aspects of the ultrastructure of the daughter sporocyst and cercaria of Podocotyle staffordi Miller, 1941 (Digenea: Opecoelidae). Norwegian Journal of Zoology 22(4), 237–252.Google Scholar
Gibson, DI (1986) Podocotyle araii sp. nov. (Digenea: Opecoelidae) from Sebastes spp. off the coast of British Columbia, with a key to the species of Podocotyle Dujardin, 1845, occurring off the Pacific coast of North America. Journal of Natural History 20, 735–743.CrossRefGoogle Scholar
Gibson, DI and Bray, RA (1982) A study and reorganization of Plagioporus Stafford, 1904 (Digenea: Opecoelidae) and related genera, with special reference to forms from European Atlantic waters. Journal of Natural History 16, 529–559.CrossRefGoogle Scholar
Gouy, M, Guindon, S and Gascuel, O (2010) SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building Molecular Biology and Evolution 27, 221–224.CrossRefGoogle Scholar
Granovitch, A and Johannesson, K (2000) Digenetic trematodes in four species of Littorina from the West Coast of Sweden. Ophelia 53(1), 55–65.CrossRefGoogle Scholar
Hunninen, AV and Cable, RM (1943) The life history of Podocotyle atomon (Rudolphi) (Trematoda: Opecoelidae). Transactions of the American Microscopical Society 62(1), 57–68.CrossRefGoogle Scholar
James, BL (1969) The Digenea of the intertidal prosobranch, Littorina saxatilis (Olivi). Journal of Zoological Systematics and Evolutionary Research 7(1), 273–316.CrossRefGoogle Scholar
Jousson, O, Bartoli, P and Pawlowski, J (1999) Molecular identification of developmental stages in Opecoelidae (Digenea). International Journal for Parasitology 29(11), 1853–1858.CrossRefGoogle ScholarPubMed
Katokhin, AV and Kornyychuk, YM (2020) Genotyping of Black Sea trematodes of the family Opecoelidae by mitochondrial markers. Marine Biological Journal 5(4), 15–27.Google Scholar
Kaliberdina, MV and Granovich, AI (2003) Infection of the mollusc Littorina saxatilis with parthenites of trematodes and their impact on a shell form: analysis of populations inhabiting the littoral coast of the White Sea. Parazitologiya 37(1), 69–86. [In Russian]Google ScholarPubMed
Køie, M (1981) On the morphology and life-history of Podocotyle reflexa (Creplin, 1825) Odhner, 1905, and a comparison of its developmental stages with those of P. atomon (Rudolphi, 1802) Odhner, 1905 (Trematoda: Opecoelidae). Ophelia 20, 17–43.Google Scholar
Layman, EM (1930) Parasitic worms from the fishes of Peter the Great Gulf. Izvestia Tikhookeanskoi Nauchno-Promyslovoi Stantsii 3, 1–120. [In Russian]Google Scholar
Levakin, IA, Nikolaev, KE and Galaktionov, KV (2012) Long-term variation in trematode (Trematoda, Digenea) component communities associated with intertidal gastropods is linked to abundance of final hosts. Hydrobiologia 706(1), 103–118.CrossRefGoogle Scholar
MacKenzie, K and Gibson, DI (1970) Ecological studies of some parasites of plaice Pleuronectes platessa L. and flounder Platichthys flesus (L.). pp. 1–42. In Taylor, A and Muller, R (Eds) Aspects of Fish Parasitology. Oxford and Edinburgh, Blackwell Scientific Publications.Google Scholar
Manter, HW (1940) Digenetic trematodes of fishes from the Galapagos Islands and neighboring Pacific. The University of Southern California publications Allan Hancock Pacific Expeditions 2(14), 325–497.Google Scholar
Martin, SB, Cutmore, SC, Ward, S and Cribb, TH (2017) An updated concept and revised composition for Hamacreadium Linton, 1920 (Opecoelidae: Plagioporinae) clarifies a previously obscured pattern of host-specificity among species. Zootaxa 4254(2), 151–187.CrossRefGoogle Scholar
Martin, SB, Huston, DC, Cutmore, SC and Cribb, TH (2019) A new classification for deep-sea opecoelid trematodes based on the phylogenetic position of some unusual taxa from shallow-water, herbivorous fishes off south-west Australia. Zoological Journal of the Linnean Society 186(2), 385–413.CrossRefGoogle Scholar
Miller, MA, Pfeiffer Wand Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. pp. 1–8. In Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA.Google Scholar
Miller, MJ (1941) A critical study of Stafford’s report on ‘Trematodes of Canadian Fishes’ based on his trematode collection. Canadian Journal of Research, Series D 19, 28–52.CrossRefGoogle Scholar
Nylander, JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala. Available at https://github.com/nylander/MrModeltest2/releases (accessed 01 July 2023).Google Scholar
Novotný, D (2019) Life cycle and diversity of Opecoelidae (Digenea) in Svalbard. 46 pp. Bc. thesis, University of South Bohemia, České Budějovice. [In Czech]Google Scholar
Odhner, T (1905) Trematoden des arktischen Gebietes. Fauna Arctica 4, 289–372. [In German]Google Scholar
Park, JT (1937) A revision of the genus Podocotyle (Allocreadiinae), with a description of eight new species from tide pool fishes from Dillon’s Beach, California Journal of Parasitology 23, 405–422.CrossRefGoogle Scholar
Pritchard, MH (1966) A revision of the genus Podocotyle (Trematoda Opecoelidae). Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere 93, 158–172.Google Scholar
Rambaut, A, Drummond, AJ, Xie, D, Baele, G and Suchard, MA (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67(5), 901–904.CrossRefGoogle ScholarPubMed
Shulman-Albova, RE (1952) On the question of the variability of the digenetic fish trematode Podocotyle atomon (Rud.) Odhner, 1905. Uchenye Zapiski Leningradslcogo Gosudarstvennogo Universiteta 141 (28), 110–126. [In Russian]Google Scholar
Sokolov, SG, Shchenkov, SV and Gordeev, II (2019) Records of opecoeline species Pseudopecoelus cf. vulgaris and Anomalotrema koiae Gibson & Bray, 1984 (Trematoda, Opecoelidae, Opecoelinae) from fish of the North Pacific, with notes on the phylogeny of the family Opecoelidae. Journal of Helminthology 93(4), 475–485.CrossRefGoogle ScholarPubMed
Sokolov, SG, Shchenkov, SV, Khasanov, FK, Kornyychuk, YM and Gordeev, II (2022). Redescription and phylogenetic assessment of Helicometra antarcticae Holloway & Bier, 1968 (Trematoda, Opecoelidae), with evidence of non-monophyletic status of the genus Helicometra Odhner, 1902. Zoosystema 44(15), 423–433.CrossRefGoogle Scholar
Szuks, H (1975) Zum Artproblem bei digenen Trematoden, dargestellt am Beispiel der Gattung Podocotyle (Dujardin, 1845) Odhner, 1905. Wissenschaftliche Zeitschrift der Pädagogischen Hoclbschule ‘Liselotte Herrmann’ Güstrow aus der Mathematische-Naturwissenschaftlichen Fakultat 2, 259–282. [In German]Google Scholar
Tamura, K, Stecher, G and Kumar, S (2021) MEGA11: Molecular evolutionary genetics analysis version 11 Molecular Biology and Evolution 38(7), 3022–3027.CrossRefGoogle ScholarPubMed
Tkach, V, Pawlowski, J and Mariaux, J (2000) Phylogenetic analysis of the suborder Plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. International Journal for Parasitology 30, 83–93.CrossRefGoogle ScholarPubMed
Tsimbaliuk, AK, Tsimbaliuk, EM and Saulina, TB (1979) Morphological outline of Podocotyle spp. from coastal fishes of the Sea of Okhotsk. All-Union Institute for Scientific and Technical Information publications 1800(79). 167–191. [In Russian]Google Scholar
Uspenskaya, AV (1963) Barents Sea benthic crustacean parasite fauna. 128 pp. Moscow, Leningrad, Publishing houses in the Soviet Union. [In Russian]Google Scholar
Zhukov, EV (1960) Endoparasitic worms of the fishes in the Sea of Japan and South-Kuril shallow waters, Trudy Zoologicheskogo Instituta ANSSR. 28, 3–146. [In Russian]Google Scholar