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Phylogenetic Position of the Hemiuroid Genus Paraccacladium Bray & Gibson, 1977 (Trematoda: Hemiuroi

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Phylogenetic Position of the Hemiuroid Genus Paraccacladium Bray & Gibson, 1977 (Trematoda: Hemiuroi Marine Biology Research ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/smar20 Phylogenetic position of the hemiuroid genus Paraccacladium Bray & Gibson, 1977 (Trematoda: Hemiuroidea) and the status of the subfamily Paraccacladiinae Bray & Gibson, 1977 Sergey G. Sokolov, Dmitry M. Atopkin & Ilya I. Gordeev To cite this article: Sergey G. Sokolov, Dmitry M. Atopkin & Ilya I. Gordeev (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, DOI: 10.1080/17451000.2021.1891252 To link to this article: https://doi.org/10.1080/17451000.2021.1891252 Published online: 10 Mar 2021. Submit your article to this journal View related articles View Crossmark data Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=smar20 MARINE BIOLOGY RESEARCH https://doi.org/10.1080/17451000.2021.1891252 ORIGINAL ARTICLE Phylogenetic position of the hemiuroid genus Paraccacladium Bray & Gibson, 1977 (Trematoda: Hemiuroidea) and the status of the subfamily Paraccacladiinae Bray & Gibson, 1977 Sergey G. Sokolov a, Dmitry M. Atopkin b and Ilya I. Gordeev c,d aA.N. Severtsov Institute of Ecology and Evolution, Moscow, Russia; bFederal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of the RAS, Vladivostok, Russia; cPacific Salmons Department, Russian Federal Research Institute of Fisheries and Oceanography, Moscow, Russia; dDepartmant of Invertebrate Zoology, Faculty of Biology, Lomonosov Moscow State University, Moscow, Russia ABSTRACT ARTICLE HISTORY In this study we tested the current taxonomic model of the trematode superfamily Received 20 December 2020 Hemiuroidea, according to which the genus Paraccacladium belongs to the family Accepted 5 February 2021 Accacoeliidae. We reconstructed the phylogeny of the hemiuroid Clade A using novel 28S KEYWORDS rRNA gene sequences of Paraccacladium sp., Derogenes varicus, Progonus muelleri and Derogenes varicus; Progonus Lampritrema miescheri as well as data available in GenBank. Based on phylogenetic data, the muelleri;·Lampritrema genus Paraccacladium should be assigned to a separate family, the Paraccacladiidae Bray & miescheri; Paraccacladiidae; Gibson, 1977 stat. nov. The morphological differences between the Paraccacladiidae and the Accacoeliidae; Derogenidae Accacoeliidae are the absence of a uroproct, anteriorly directed diverticula of intestinal caeca, and the position of Mehlis’ gland, posterior or postero-lateral to the ovary. Phylogenetic analysis indicates a sister relationship between the Derogenidae and the Sclerodistomidae. It also shows that the Paraccacladiidae, on the one hand, and a group of families, the Accacoeliidae, Hirudinellidae and Syncoeliidae, on the other, share the most recent common ancestor. Our data support the hypothesis that the genus Lampritrema is affiliated to the Hirudinellidae. Genetic divergence between North Atlantic and North Pacific isolates of D. varicus was also determined. Introduction on a short fragment of the 18S rRNA gene (Pankov Paraccacladium Bray & Gibson, 1977 is a small genus of et al. 2006) did not reveal any direct phylogenetic hemiuroid trematodes. It contains only two species, relationships between the Paraccacladiinae and the Paraccacladium jamiesoni Bray & Gibson, 1977 (type nominotypical subfamily of the Accacoeliidae. At the species) and Paraccacladium leontjevae (Korotaeva, same time, the Accacoeliinae together with the 1976) (see Bray and Gibson 1977). Paraccacladium families Derogenidae, Didymozoidae, Hirudinellidae, jamiesoni is typical of the North and Central Atlantic Sclerodistomidae and Syncoeliidae were found to (Bray and Gibson 1977; Campbell et al. 1980; Gaevs- belong to a monophyletic group (Clade A) in 28S kaya and Aleshkina 1983; Scott 1987; Gaevskaya rRNA gene-based phylogeny of the Hemiuroidea 2002) but was also recorded in the northwest-central (Sokolov et al. 2019). region of the North Pacific (Machida 1985). Paraccacla- During the course of a parasitological survey of dium leontjevae was found in the South Pacific (Koro- fishes and amphipods caught in the North-west taeva 1976) and South Atlantic (Aleshkina and Pacific and the White Sea, we found Paraccacladium Gaevskaya 1985). sp., as well as the derogenids Derogenes varicus In the current taxonomic model of the Hemiuroidea, (Müller, 1784) (North Pacific isolate) and Progonus Paraccacladium is a member of the monotypic subfam- muelleri (Levinsen, 1881), and a hirudinellid Lampri- ily Paraccacladiinae Bray & Gibson, 1977 of the family trema miescheri (Zschokke, 1890). These trematodes Accacoeliidae Odhner, 1911 (see Gibson 2002). have never been studied with the use of 28S rDNA However, the results of phylogenetic analysis based sequence data. The goal of the present study was to CONTACT ILYA I. GORDEEV [email protected] Pacific Salmons Department, Russian Federal Research Institute of Fisheries and Oceanography, V. Krasnoselskaya Str. 17, Moscow, 107140, Russia Departmant of Invertebrate Zoology, Faculty of Biology, Lomonosov Moscow State University, Leninskie Gory 1/12, Moscow, 119234, Russia Supplemental data for this article can be accessed https://doi.org/10.1080/17451000.2021.1891252 © 2021 Informa UK Limited, trading as Taylor & Francis Group Published online 10 Mar 2021 2 S. G. SOKOLOV ET AL. reveal the taxonomic status of the subfamily Paracca- descriptions are given in micrometres, unless stated cladiinae based on the 28S rRNA gene-based phyloge- otherwise. Drawings of Derogenes varicus, Lampritrema netic analysis of the trematodes from our collections miescheri and Progonus muelleri are in the Supplemen- and the GenBank (NCBI) dataset. tary Materials (Figures S1–S3). The identification of these species was undertaken following Margolis (1962) and Gibson (1996). Slides with trematodes Materials and methods were deposited in the Museum of Helminthological Collections at the Center of Parasitology of the A.N. Sample collection and morphological Severtsov Institute of Ecology and Evolution (IPEE observation RAS) in Moscow, Russia. Specimens for molecular The trematodes were collected during a parasitological analysis were fixed in 96% ethanol and stored at examination of six species of North Pacific fishes: Apto- −18°C. cyclus ventricosus (Pallas, 1769) (Actinopterygii: Cyclop- teridae), total length 2.9–25 cm, weight 12–1385 g; DNA extraction, amplification and sequencing, Icichthys lockingtoni Jordan & Gilbert, 1880 (Actinopter- and phylogenetic analysis ygii: Centrolophidae), 42 cm, 512 g; Leuroglossus schmidti Rass, 1955 (Actinopterygii: Bathylagidae), Total DNA was extracted from the worms fixed in 96% 11.1–17.2 cm, 8–12 g; Brama japonica Hilgendorf, ethanol using the ‘hot shot’ technique (Truett 2006). 1878 (Actinopterygii: Bramidae), 37.7–47.0 cm, 1086– The polymerase chain reaction (PCR) was used to 1327 g; Eumicrotremus fedorovi Mandrytsa, 1991 (Acti- amplify V4 region of 18S rRNA gene using the nopterygii: Cyclopteridae), 6.7–8.9 сm, 12.4–45.2 g; and primers 18S-8 (5’-GCA GCC GCG GTA ACT CCA GC-3’) Antimora microlepis Bean, 1890 (Actinopterygii: and 18S-A27 (5’-CCA TAC AAA TGC CCC CGT CTG-3’) Moridae), 11.5–45.2 cm, 4–1350 g. as previously described (Littlewood and Olson 2001). Aptocyclus ventricosus, I. lockingtoni and L. schmidti The initial PCR was performed in a total volume of 25 were caught from the research vessel Professor Kaga- µl and contained 0.25 mM of each primer, ∼10 ng of novsky between 31 May 2018 and 7 July 2018 in the total DNA in water and 12.5 µl of 2× Go Taq Green open waters of the North-west Pacific (40–50°N, 147– Master mix (Promega). Amplification of a 400 base 167°E) (Gordeev et al. 2018; Gordeev and Sokolov pair (bp) fragment of 18S rDNA was performed in a 2020b). Brama japonica was caught from the research GeneAmp 9700 (Applied Biosystems, USA) with a 5 vessel Professor Kaganovsky on 27 September 2019 in min denaturation at 96°C, 35 cycles of 1 min at 96°C, the Bering Sea (53°38′05′′N, 169°23′05′′E) (Gordeev 20 s at 58°C and 1 min at 72°C and a 2 min extension et al. 2019). Antimora microlepis was caught in two at 72°C. Negative and positive controls with the use localities: near Japan (41–42°N, 143–144°E) between of both primers were included. 7 and 10 June 2016 at a depth from 560–961 m and The 28S rRNA gene was amplified with the primers from RV Professor Levanidov on 2 September 2018 DIG12 (5’-AAG CAT ATC ACT AAG CGG-3’) and 1500R near the Kuril Islands (49°34′N, 156°19′E) at a depth (5’-GCT ATC CTG AGG GAA ACT TCG-3’) as previously of 550 m. Eumicrotremus fedorovi was caught near described (Tkach et al. 2003). The master mix for the Simushir Island (47°13′04′′N, 152°27′06′′E; 46°44′08′′N, PCR reaction was identical to that described above 151°52′05′′E) on 23–24 March 2017 at a depth of 230 for 18S rDNA. Amplification of a 1200 bp fragment m (Gordeev and Sokolov 2020a). Specimens of An. of 28S rRNA gene was carried out in a GeneAmp microlepis and E. fedorovi were frozen, and then 9700 (Applied Biosystems, USA) with a 3 min dena- thawed and dissected in the laboratory, while the turation at 94°C, 40 cycles of 30 s at 94°C, 30 s at other specimens were dissected directly after capture. 55°C and 2 min at 72°C and a 7 min extension at Trematodes were also isolated from the amphipod 72°C. Negative and positive controls with the use of Caprella septentrionalis Krøyer, 1838 (Amphipoda: both primers were included. A ribosomal ITS1-5.8S- Caprellidae) collected near the White Sea Biological ITS2 fragment was amplified with primers BD1 (5’- Station of Lomonosov Moscow State University GTC GTA ACA AGG TTT CCG TA-3’) and BD2 (5’-TAT (Great Salma Straight, White Sea, 66°33′01′′N, 33° GCT TAA ATT CAG CGG GT-3’) (Luton et al. 1992) 09′10′′E) on 19 July 2019. with an annealing temperature of 54°C.
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