Trans-Arctic distribution of marine fish digenean Progonus muelleri (Derogenidae) tested by molecular data
- Authors: Krupenko D.Y.1,2, Kremnev G.A.1, Gonchar A.G.1,2, Skobkina O.A.1, Regel K.V.3
-
Affiliations:
- Zoological Institute of the Russian Academy of Sciences
- Saint Petersburg University
- Institute of the Biological Problems of the North, Far Eastern Branch of the Russian Academy of Sciences
- Issue: Vol 59, No 1 (2025)
- Pages: 3-26
- Section: Articles
- URL: https://ruspoj.com/0031-1847/article/view/682981
- DOI: https://doi.org/10.31857/S0031184725010016
- EDN: https://elibrary.ru/UMTSPG
- ID: 682981
Cite item
Abstract
In the digenean superfamily Hemiuroidea, a number of species are registered from a wide geographic range including the Arctic, Atlantic and Pacific Oceans. However, these distributions have not yet been confirmed with the molecular methods. In the present study, we performed molecular analysis of Progonus muelleri (Levinsen, 1881) (Derogenidae) from distant regions: the European sub-Arctic (the White, Barents and Pechora Seas) and the Pacific Northwest (the Sea of Okhotsk and the Pacific coast of the northern Kuril Islands). Two genetic lineages within P. muelleri, PM1 and PM2, are proved to occur in sympatry in the European sub-Arctic. We found minor differences in their maritae structure, and thus suppose they represent two pseudocryptic species. PM1 was also registered in the Pacific Northwest (PM1b) where it has differences in cox1 gene from the European sub-Arctic lineage (PM1a). The intramolluscan life-cycle stages of P. muelleri from the Sea of Okhotsk are described and compared with the ones from the White Sea. We hypothesize that PM1a, PM1b and PM2 are three distinct species, but this should be further tested.
Keywords
Full Text

About the authors
D. Yu. Krupenko
Zoological Institute of the Russian Academy of Sciences; Saint Petersburg University
Author for correspondence.
Email: krupenko.d@gmail.com
Russian Federation, Universitetskaya emb., 1, Saint Petersburg, 199034; Universitetskaya emb., 7/9, Saint Petersburg, 199034
G. A. Kremnev
Zoological Institute of the Russian Academy of Sciences
Email: krupenko.d@gmail.com
Russian Federation, Universitetskaya emb., 1, Saint Petersburg, 199034
A. G. Gonchar
Zoological Institute of the Russian Academy of Sciences; Saint Petersburg University
Email: krupenko.d@gmail.com
Russian Federation, Universitetskaya emb., 1, Saint Petersburg, 199034; Universitetskaya emb., 7/9, Saint Petersburg, 199034
O. A. Skobkina
Zoological Institute of the Russian Academy of Sciences
Email: krupenko.d@gmail.com
Russian Federation, Universitetskaya emb., 1, Saint Petersburg, 199034
K. V. Regel
Institute of the Biological Problems of the North, Far Eastern Branch of the Russian Academy of Sciences
Email: krupenko.d@gmail.com
Russian Federation, Portovaya str., 18, Magadan, 685000
References
- Blasco‐Costa I., Waters J.M., Poulin R. 2012. Swimming against the current: genetic structure, host mobility and the drift paradox in trematode parasites. Molecular ecology 21 (1): 207–217. https://doi.org/10.1111/j.1365-294X.2011.05374.x
- Borges L.M., Treneman N.C., Haga T., Shipway J.R., Raupach M.J., Altermark B., Carlton J.T. 2022. Out of taxonomic crypsis: a new trans-arctic cryptic species pair corroborated by phylogenetics and molecular evidence. Molecular Phylogenetics and Evolution 166: 107312. https://doi.org/10.1016/j.ympev.2021.107312
- Bouckaert R.R., Drummond A.J. 2017. bModelTest: Bayesian phylogenetic site model averaging and model comparison. BMC Evolutionary Biology 17: 1–11. https://doi.org/10.1016/j.ympev.2021.107312
- Bouckaert R., Vaughan T.G., Barido-Sottani J., Duchêne S., Fourment M., Gavryushkina A., Heled J., Jones G., Kühnert D., De Maio N., Matschiner M., Mendes F.K., Müller N.F., Ogilvie H.A., du Plessis L., Popinga A., Rambaut A., Rasmussen D., Siveroni I., Suchard M.A., Wu C-H., Xie D., Zhang C., Stadler T., Drummond, A.J. 2019. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology 15 (4): e1006650. https://doi.org/10.1016/j.ympev.2021.107312
- Bouguerche C., Huston D.C., Cribb T.H., Karlsbakk E., Ahmed M., Holovachov O. 2023. Hidden in the fog: morphological and molecular characterisation of Derogenes varicus sensu stricto (Trematoda, Derogenidae) from Sweden and Norway, and redescription of two poorly known Derogenes species. Parasite, 30: 35. https://doi.org/10.1051/parasite/2023030
- Bouguerche C., Huston D.C., Karlsbakk E., Ahmed M., Holovachov O. 2024. Untangling the Derogenes varicus species complex in Scandinavian waters and the Arctic: description of Derogenes abba n. sp. (Trematoda, Derogenidae) from Hippoglossoides platessoides and new host records for D. varicus (Müller, 1784) sensu stricto. Parasite 31: 26. https://doi.org/10.1051/parasite/2024024
- Bowles J., Hope M., Tiu W.U., Liu X., McManus D.P. 1993. Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum. Acta Tropica 55 (4): 217–229. https://doi.org/10.1016/0001-706X(93)90079-Q
- Bray R.A. 1979. Digenea in marine fishes from the eastern seaboard of Canada. Journal of Natural History 13 (4): 399–431. https://doi.org/10.1080/00222937900770331
- Bray R.A., Cutmore S.C., Cribb T.H. 2022 A paradigm for the recognition of cryptic trematode species in tropical Indo-west Pacific fishes: The problematic genus Preptetos (Trematoda: Lepocreadiidae). International Journal for Parasitology 52 (2–3): 169–203. https://doi.org/10.1016/j.ijpara.2021.08.004
- Briggs J.C. 2003. Marine centres of origin as evolutionary engines. Journal of Biogeography 30: 1–18. https://doi.org/10.1046/j.1365-2699.2003.00810.x
- Brinkmann A.J. 1975. Trematodes from Greenland. Meddelelser om Grønland 205 (2): 1–88.
- Carr C.M., Hardy S.M., Brown T.M., Macdonald T.A., Hebert P.D. 2011. A tri-oceanic perspective: DNA barcoding reveals geographic structure and cryptic diversity in Canadian polychaetes. PLoS One 6 (7): e22232. https://doi.org/10.1371/journal.pone.0022232
- Chaban E., Ekimova I., Stanovova M., Schepetov D. 2023. Integrative Analysis of Retusa pertenuis (Heterobranchia: Cephalaspidea) from Arctic and Russian Far East Seas with Discussion of Its Morphology, Validity and Population Structure. Diversity 15 (9): 974. https://doi.org/10.3390/d15090974
- Clement M., Snell Q., Walke P., Posada D., Crandall K. 2002. TCS: estimating gene genealogies. Parallel and Distributed Processing Symposium, International Proceedings 2: 184. https://doi.org/10.1109/IPDPS.2002.1016585
- Cribb T.H., Adlard R.D., Bray R.A. 1998. A DNAbased demonstration of a three-host life-cycle for the Bivesiculidae (Platyhelminthes: Digenea). International Journal for Parasitology 28 (11): 1791–1795. https://doi.org/10.1016/S0020-7519(98)00127-1
- Galaktionov K.V., Blasco-Costa I., Olson P.D. 2012. Life cycles, molecular phylogeny and historical biogeography of the ‘pygmaeus’ microphallids (Digenea: Microphallidae): widespread parasites of marine and coastal birds in the Holarctic. Parasitology 139 (10): 1346–1360. https://doi.org/10.1017/s0031182012000583
- Galaktionov K.V., Solovyeva A.I., Blakeslee A.M., Skírnisson K. 2023. Overview of renicolid digeneans (Digenea, Renicolidae) from marine gulls of northern Holarctic with remarks on their species statuses, phylogeny and phylogeography. Parasitology 150 (1): 55–77. https://doi.org/10.1017/S0031182022001500
- Galaktionov K.V., Gonchar A., Postanogova D., Miroliubov A., Bodrov S.Y. 2024a. Parvatrema spp. (Digenea, Gymnophallidae) with parthenogenetic metacercariae: Diversity, distribution and host specificity in the palaearctic. International Journal for Parasitology 54 (7): 333–355. https://doi.org/10.1016/j.ijpara.2024.02.002
- Galaktionov K.V., Solovyeva A.I., Miroliubov A.A., Romanovich A.E., Skírnisson K. 2024b. Untangling the “Renicola somateria” (Digenea, Renicolidae) Muddle: Actual Number of Species and Their Distribution and Transmission in the Holarctic. Diversity 16 (7): 402. https://doi.org/10.3390/d16070402
- Gharbi K., Bouguerche C., Ahmed M., Pérez-Ponce de León G., Tazerouti F. 2024. Redescription and Molecular Characterisation of Derogenes ruber Lühe, 1900 (Hemiuroidea: Derogenidae) from Chelidonichthys lastoviza (Scorpaeniformes: Triglidae) in the Western Mediterranean. Acta Parasitologica 69 (1): 309–323. https://doi.org/10.1007/s11686-023-00749-z
- Gonchar A., Galaktionov K.V. 2020. New data support phylogeographic patterns in a marine parasite Tristriata anatis (Digenea: Notocotylidae). Journal of Helminthology 94: 1–5. https://doi.org/10.1017/S0022149X19000786
- Gonchar A., Galaktionov K.V. 2022. The Pacific Notocotylus atlanticus (Digenea: Notocotylidae). Parasitology International 88: 102559. https://doi.org/10.1016/j.parint.2022.102559
- Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic biology 59(3): 307–321. https://doi.org/10.1093/sysbio/syq010
- Huyse T., Poulin R., Theron A. 2005. Speciation in parasites: a population genetics approach. Trends in Parasitology 21 (10): 469–475. doi: 10.1016/j.pt.2005.08.009
- Issaitschikov I.M. 1933 Contributions to the knowledge of parasitic helminths of some groups of vertebrates in the Russian Arctic. A. Trematodes (part 2). Trudy Gosudarstvennogo Okeanograficheskogo Instituta 3 (1): 3–44. [In Russian with English summary].
- Kienberger K., Carmona L., Pola M., Padula V., Gosliner T.M., Cervera J.L. 2016. Aeolidia papillosa (Linnaeus, 1761) (Mollusca: Heterobranchia: Nudibranchia), single species or a cryptic species complex? A morphological and molecular study. Zoological Journal of the Linnean Society 177 (3): 481–506. https://doi.org/10.1111/zoj.12379
- Køie M. 1979. On the morphology and life-history of Derogenes varicus (Müller, 1784) Looss, 1901 (Trematoda, Hemiuridae). Zeitschrift für Parasitenkunde 59: 67–78. https://doi.org/10.1007/BF00927847
- Králová-Hromadová I., Špakulová M., Horáčková E., Turčeková L., Novobilský A., Beck R., Koudela B., Marinculić A., Rajský D., Pybus M. 2008. Sequence analysis of ribosomal and mitochondrial genes of the giant liver fluke Fascioloides magna (Trematoda: Fasciolidae): intraspecific variation and differentiation from Fasciola hepatica. Journal of Parasitology 94 (1): 58–67. https://doi.org/10.1645/GE-1324.1
- Krupenko D., Kremnev G., Gonchar A., Uryadova A., Miroliubov A., Krapivin V., Skobkina O., Gubler A., Knyazeva O. 2022. Species complexes and life cycles of digenetic trematodes from the family Derogenidae. Parasitology. 149 (12): 1590–1606. https://doi.org/10.1017/S003118202200110X
- Laakkonen H.M., Hardman M., Strelkov P., Väinölä R. 2021. Cycles of trans‐Arctic dispersal and vicariance, and diversification of the amphi‐boreal marine fauna. Journal of Evolutionary Biology 34 (1): 73–96. https://doi.org/10.1111/jeb.13674
- Laakkonen H.M., Strelkov P., Väinölä R. 2015. Molecular lineage diversity and inter‐oceanic biogeographical history in Hiatella (Mollusca, Bivalvia). Zoologica Scripta 44 (4): 383–402. https://doi.org/10.1111/zsc.12105
- Leigh J.W., Bryant D. 2015. PopART: full‐feature software for haplotype network construction. Methods in Ecology & Evolution 6 (9): 1110–1116. https://doi.org/10.1111/2041-210X.12410
- Levinsen G.M.R. 1881. Bidrag til kundskap om Gronlands trematodfauna. Oversigt over det kongelige Dansk videnskadernes Selskabs Forhandlinger 23: 52–84. [In Danish].
- Miura O., Takisawa S. 2024. Biogeography of larval trematodes in the freshwater snail, Semisulcospira libertina: a comparison of the morphological and molecular approaches. Parasitology International 102: 102924. https://doi.org/10.1016/j.parint.2024.102924
- Morgan J.A.T., Blair D. 1995. Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: an aid to establishing relationships within the 37-collarspine group. Parasitology 111 (5): 609–615. https://doi.org/10.1017/S003118200007709X
- Odhner T. 1905. Die Trematoden des arktischen Gebietes. Fauna Arctica 4: 289–372. [In German].
- Olson P.D., Cribb T.H., Tkach V.V., Bray R.A., Littlewood D.T.J. 2003. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33 (7): 733–755. https://doi.org/10.1016/S0020-7519(03)00049-3
- Pérez-Ponce de León G., Poulin R. 2018. An updated look at the uneven distribution of cryptic diversity among parasitic helminths. Journal of Helminthology 92 (2): 197–202. https://doi.org/10.1017/S0022149X17000189
- Polyansky Y.I. 1955. Studies on the parasitology of the fish in the northern seas of the USSR. Parasites of fish of the Barents Sea. Trudy Zoologicheskogo Instituta 19: 5–170. [In Russian: English translation (1966) Israel Program for Scientific Translations, Cat. No. 1655.].
- Rambaut A., Drummond A.J., Xie D., Baele G., Suchard M.A. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67 (5): 901–904. https://doi.org/10.1093/sysbio/syy032
- Rysgaard S., Boone W., Carlson D., Sejr M.K., Bendtsen J., Juul‐Pedersen T., Lund H., Meire L., Mortensen J. 2020. An updated view on water masses on the pan‐west Greenland continental shelf and their link to proglacial fjords. Journal of Geophysical Research: Oceans 125 (2): e2019JC015564. https://doi.org/10.1029/2019JC015564
- Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden S., Saalfeld S., Schmid B., Tinevez J.Y., White D.J., Hartenstein V., Eliceiri K., Tomancak P., Cardona A. 2012. Fiji: an open-source platform for biological-image analysis. Nature Methods 9 (7): 676–682. https://doi.org/10.1038/nmeth.2019
- Sokolov S.G., Atopkin D.M., Gordeev I.I. 2021. Phylogenetic position of the hemiuroid genus Paraccacladium Bray & Gibson, 1977 (Trematoda: Hemiuroidea) and the status of the subfamily Paraccacladiinae Bray & Gibson, 1977. Marine Biology Research 17 (1): 31–40. https://doi.org/10.1080/17451000.2021.1891252
- Tamura K., Stecher G., Kumar S. 2021. MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution 38 (7): 3022–3027. https://doi.org/10.1093/molbev/msab120
- Tkach V., Grabda-Kazubska B., Pawlowski J., Swiderski Z. 1999. Molecular and morphological evidence for close phylogenetic affinities of the genera Macrodera, Leptophallus, Metaleptophallus and Paralepoderma [Digenea, Plagiorchiata]. Acta Parasitologica 44 (3): 170–179.
- Tsuchida K., Rauque C., Viozzi G., Flores V., Urabe M. 2022. First report of post-cyclic transmission in trematodes: Derogenes lacustris (Digenea: Hemiuroidea) in Patagonian freshwater fishes. Parasitology 149 (2): 234–238. https://doi.org/10.1017/S0031182021001736
- Vermeij G.J. 1991. Anatomy of an invasion: The trans-Arctic interchange. Paleobiology 17: 281–307. https://doi.org/10.1017/S0094837300010617
- WoRMS. 2024. Progonus muelleri (Levinsen, 1881) Looss, 1899. https://marinespecies.org/aphia.php?p=taxdetails&id=109275 on 2024-11-13.
- Zhukov E.V. 1963 Parasite fauna of fish in Chukotka. Part II. Endoparasites of marine and fresh-water fish. Parazitologicheski Sbornik 21: 96–139. [In Russian with English summary].
Supplementary files
