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Phylogeny of two accacoeliid species (Digenea: Hemiuroidea) ex Mola mola (Linnaeus, 1758) (Tetraodontiformes: Molidae) from Northwest Pacific, with first molecular data on Odhnerium Yamaguti, 1934

Published online by Cambridge University Press:  14 May 2025

S.G. Sokolov
Affiliation:
A.N. Severtsov Institute of Ecology and Evolution of RAS, Leninskiy Pros. 33, Moscow 119071, Russia
I.I. Gordeev
Affiliation:
Pacific Salmon Department, Russian Federal Research Institute of Fisheries and Oceanography, Okruzhnoy Pr. 19, Moscow 105187, Russia Department of Invertebrate Zoology, Faculty of Biology, Lomonosov Moscow State University, Leninskie Gory 1/12, Moscow 119234, Russia
D.M. Atopkin*
Affiliation:
Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of Russian Academy of Sciences, Vladivostok, Russia
*
Corresponding author: D.M. Atopkin; Email: atop82@gmail.com

Abstract

Accacoeliid digeneans associated with fish of the family Molidae exhibit enigmatically high taxonomic diversity. However, the phylogenetic relationships between species within this digenean taxon are poorly understood. In the present study, the first nuclear 28S rRNA gene, ITS2 region of nuclear DNA, and mitochondrial cox1 gene sequence datasets were obtained for two members of the Accacoeliidae, a type and only species of the genus Odhnerium Yamaguti 1934 and an unidentified Accacladocoelium sp. collected from Mola mola (Linnaeus, 1758) off Iturup Island. Analyses of molecular differentiation and phylogenetic relationships indicate that Accacladocoelium sp. is a sister species to Accacladocoelium nigroflavum (Rudolphi, 1819). The genus Odhnerium is closely related to Tetrochetus Looss, 1912, on the 28S rRNA gene-based phylogenetic tree. Results of phylogenetic analysis based on both the mitochondrial cox1 gene and the concatenated ribosomal ITS2 region and cox1 gene of mtDNA show that the genus Odhnerium is close to the A. nigroflavum + Accacladocoelium sp. clade. In turn, the genus Accacladocoelium does not have monophyletic status in the trees reconstructed from these data.

Type
Short Communication
Copyright
© The Author(s), 2025. Published by Cambridge University Press

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References

Ahuir-Baraja, AE, Fraija-Fernández, N, Raga, JA and Montero, FE (2015a) Molecular and morphological differentiation of two similar species of Accacoeliidae (Digenea): Accacladocoelium macrocotyle and A. nigroflavum from sunfish, Mola mola. Journal of Parasitology 101, 231235. doi: 10.1645/14-496.1.CrossRefGoogle Scholar
Ahuir-Baraja, AE, Padros, F, Palacios-Abella, JF, Raga, JA and Montero, FE (2015b) Accacoelium contortum (Trematoda: Accacoeliidae) a trematode living as a monogenean: Morphological and pathological implications. Parasites & Vectors 8, 540. doi: 10.1186/s13071-015-1162-1.CrossRefGoogle Scholar
Atopkin, DM, Semenchenko, AA, Solodovnik, DA and Ivashko, YI (2023) A definitive host from the Russian Far East, and unexpected phylogeny of Azygiidae within Digenea, as inferred from mitogenome sequences. Journal of Helminthology 97, e69. doi: 10.1017/S0022149X23000500.CrossRefGoogle ScholarPubMed
Bouguerche, С, Huston, ВС, Cribb, TH, Karlsbakk, E, Ahmed, M and 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. doi: 10.1051/parasite/2023030.CrossRefGoogle ScholarPubMed
Bowles, J, Blair, D and McManus, DP (1995) A molecular phylogeny of the human schistosomes. Molecular Phylogenetics and Evolution 4, 103109. doi: 10.1006/mpev.1995.1011.CrossRefGoogle ScholarPubMed
Bray, RA and Gibson, DI (1977) The Accacoeliidae (Digenea) of fishes from the North-East Atlantic. Bulletin of the British Museum (Natural History), (Zoology Series) 31, 5399.Google Scholar
Bykhovskaya-Pavlovskaya IE (1985) Fish Parasites: A Guide to Learning. Leningrad: Nauka.Google Scholar
Caldera, EJ, Whitney, JL, Nyegaard, M, Ostalé-Valriberas, E, Kubicek, L and Thys, TM (2020) Genetic insights regarding the taxonomy, phylogeography and evolution of ocean sunfishes (Molidae: Tetraodontiformes). In Thys, TM, Hays, GC and Houghton, JDR (eds), The Ocean Sunfishes: Evolution, Biology and Conservation. Boca Raton: CRC Press, 3754.CrossRefGoogle Scholar
Claxton, AT, Fuehring, AD, Andres, MJ, Moncrief, TD and Curran, S (2017) Parasites of the Vermilion Snapper, Rhomboplites aurorubens (Cuvier), from the Western Atlantic Ocean. Comparative Parasitology 84, 114. doi: 10.1654/1525-2647-84.1.1.CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) jModeltest2: More models, new heuristics and parallel computing. Nature Methods 9, 772. doi: 10.1038/nmeth.2109.CrossRefGoogle Scholar
Fernández, I, Oyarzún, C, Valenzuela, A, Burgos, C, Guaquín, V and Campos, V (2016) Parásitos del pez luna Mola mola (Pisces: Molidae). Primer registro en aguas de la costa centro sur de Chile. Gayana 80, 192197. doi: 10.4067/S0717-65382016000200192.Google Scholar
Gharbi, K, Bouguerche, C, Ahmed, M, de León G, Pérez-Ponce and 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, 309323. doi: 10.1007/s11686-023-00749-z.CrossRefGoogle ScholarPubMed
Gibson, DI (2002) Family Accacoeliidae Odhner, 1911. In Gibson, DI, Jones, A and Bray, RA (eds), Keys to the Trematoda , Volume 1. London: CAB International, 341347. doi: 10.1079/9780851995472.034.CrossRefGoogle Scholar
Huelsenbeck, JP, Ronquist, F, Nielsen, R and Bollback, JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294, 23102314. doi: 10.1126/science.1065889.CrossRefGoogle ScholarPubMed
Klimpel, S, Kuhn, T, Münster, J, Dörge, DD, Klapper, R and Kochmann, J (2019) Parasites of Marine Fish and Cephalopods. New York: Springer International Publisher. doi: 10.1007/978-3-030-16220-7.CrossRefGoogle Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0. Molecular Biology and Evolution 33, 18701874. doi: 10.1093/molbev/msw054.CrossRefGoogle ScholarPubMed
Linton, E (1898) Notes on trematode parasites of fishes. Proceedings of the United States National Museum 20, 507548. doi: 10.5479/si.00963801.20-1133.507.CrossRefGoogle Scholar
Littlewood, DTJ and Olson, PD (2001) Small subunit rDNA and the Platyhelminthes: Signal, noise, conflict and compromise. In Littlewood, DTJ and Bray, RA (eds), Interrelationships of Platyhelminthes. London: Taylor & Francis, 262278.Google Scholar
Louvard, C, Yong, RQ, Cutmore, SC and Cribb, TH (2024) The oceanic pleuston community as a potentially crucial life-cycle pathway for pelagic fish-infecting parasitic worms. International Journal for Parasitology 54, 267278. doi: 10.1016/j.ijpara.2023.11.001.CrossRefGoogle ScholarPubMed
Luque, JL, Cruces, C, Chero, J, Paschoal, F, Alves, PV, Silva, AC, Sanchez, L and Iannacone, J (2016) Checklist of metazoan parasites of fishes from Peru. Lista de verificación de los metazoos parásitos de peces de Perú. Neotropical Helminthology 10, 301375.CrossRefGoogle Scholar
Luque, J and Oliva, M (1993) Trematodes of marine fishes from the Peruvian faunistic province (Perú and Chile), with description of Lecithochirium callaoensis n. sp. and new records. Revista de Biologia Marina 28, 271286.Google Scholar
Luton, K, Walker, D and Blair, D (1992) Comparisons of ribosomal internal transcribed spacers from two congeneric species of flukes (Platyhelminthes: Trematoda: Digenea). Molecular and Biochemical Parasitology 56, 323327. doi: 10.1016/0166-6851(92)90181-I.CrossRefGoogle ScholarPubMed
Manter, HW (1954) Some digenetic trematodes from fishes of New Zealand. Transactions of the Royal Society of New Zealand 82, 475568.Google Scholar
Matejusova, I and Cunningham, CO (2004) The first complete monogenean ribosomal RNA gene operon: Sequence and secondary structure of the Gyrodactylus salaris Malmberg, 1957, large subunit ribosomal RNA gene // Journal of Parasitology 90, 146151. doi: 10.1645/GE-111R3.Google ScholarPubMed
Miura, F, Uematsu, C, Sakaki, Y and Ito, T (2005) A novel strategy to design highly specific PCR primers based on the stability and uniqueness of 3′-end subsequences. Bioinformatics 21, 43634370. doi: 10.1093/bioinformatics/bti716.CrossRefGoogle ScholarPubMed
Nyegaard, M, Sawai, E, Gemmell, N, Gillum, J, Loneragan, NR, Yamanoue, Y and Stewart, AL (2017) Hiding in broad daylight: Molecular and morphological data reveal a new ocean sunfish species (Tetrodontiformes: Molidae) that has eluded recognition. Zoological Journal of the Linnean Society 182, 128. doi: 10.1093/zoolinnean/zlx040.Google Scholar
Olson, PD, Cribb, TH, Tkach, VV, Bray, RA and Littlewood, DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733755. doi: 10.1016/S0020-7519(03)00049-3.CrossRefGoogle ScholarPubMed
Pratt, I and McCauley, JE (1961) Trematodes of the Pacific Northwest. An Annotated Catalog. Corvallis: Oregon State University Press.Google Scholar
Sokolov, SG, Gordeev, II and Atopkin, DM (2016) Redescription of trematode Gonocerca muraenolepisi Paruchin et Ljadov, 1979 (Hemiuroidea: Derogenidae), a body cavity parasite of Antarctic fishes, with a discussion of its phylogenetic position. Invertebrate Zoology 13, 191202. doi: 10.15298/invertzool.13.2.02.CrossRefGoogle Scholar
Sokolov, SG, Atopkin, DM and Gordeev, II (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, 3140. doi: 10.1080/17451000.2021.1891252.CrossRefGoogle Scholar
Sokolov, SG, Atopkin, DM, Gordeev, II and Shedko, MB (2017) Phylogenetic position of the genus Gonocerca Manter, 1925 (Trematoda, Hemiuroidea), based on partial sequences of 28S rRNA gene and a reconsideration of taxonomic status of Gonocercinae Skrjabin et Guschanskaja, 1955. Parasitology International 67, 7478. https://doi.org/10.1016/j.parint.2017.03.007.CrossRefGoogle Scholar
Timon-David, P and Musso, JJ (1971) Les trématodes digènes du poisson-lune (Mola mola) dans le Golfe de Marseille (Accacoeliidae et Didymozoidae). Annales de Parasitologie Humaine et Comparée 46, 233256.Google Scholar
Tkach, VV, Littlewood, DTJ, Olson, PD, Kinsella, JM and Swiderski, Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56, 115. doi: 10.1023/A:1025546001611.CrossRefGoogle ScholarPubMed
Tsuchida, K, Flores, V, Viozzi, G, Rauque, C and Urabe, M (2021a) Hemiuroidean trematodes from freshwater Patagonian fishes: Description of a new species, distribution and molecular phylogeny. Parasitology Research 120, 12191232. doi: 10.1007/s00436-020-06939-2.CrossRefGoogle Scholar
Tsuchida, K, Urabe, M, Viozzi, G, Raucue, C and Flores, V (2021b) A new species of hemiuroidean trematode from Hatcheria macraei (Siluriformes, Trichomycteridae) and Heleobia hatchery (Gastropoda, Cochliopidae) in a Patagonian River. Parasitology Research 120, 25232532. doi: 10.1007/s00436-021-07210-y.CrossRefGoogle Scholar
Villalba, SC and Fernández, JB (1985) Parásitos de Mola ramsayi (Giglioli, 1883) (Pisces: Molidae) en Chile. Boletín de la Sociedad de Biologia de Concepción 56, 7178.Google Scholar
WoRMS (2025) World Register of Marine Species. Accacoeliidae Odhner, 1911. Available at https://www.marinespecies.org/ (accessed March 20, 2025).Google Scholar
Wu, Y-A, Gao, J-W, Cheng, X-F, Xie, M, Yuan, X-P, Liu, D and Song, R (2020) Characterization and comparative analysis of the complete mitochondrial genome of Azygia hwangtsiyui Tsin, 1933 (Digenea), the first for a member of the family Azygiidae. ZooKeys 945, 116. doi: 10.3897/zookeys.945.49681.CrossRefGoogle ScholarPubMed
Yamaguti, S (1934) Studies on the helminth fauna of Japan. Part 2. Trematodes of fishes. I. Japanese Journal of Zoology 5, 249541.Google Scholar
Zhang, S, S-F, Liu and Yang, T-B (2016) Two new records of genera, with redescription of Accacoelium contortum (Ruldolphi, 1819) and Accacladocoelium petasiporum (Odhner, 1928) (Digenea: Accacoeliidae). Acta Hydrobiologica Sinica 40, 10511055. doi: 10.7541/2016.136.Google Scholar