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Redescription and Supplementary Molecular Characteristics of Aspidogaster Ijimai Kawamura, 1915 (Trematoda, Aspidogastrea, Aspid

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Redescription and Supplementary Molecular Characteristics of Aspidogaster Ijimai Kawamura, 1915 (Trematoda, Aspidogastrea, Aspid Parasitology International 71 (2019) 167–176 Contents lists available at ScienceDirect Parasitology International journal homepage: www.elsevier.com/locate/parint Redescription and supplementary molecular characteristics of Aspidogaster ijimai Kawamura, 1915 (Trematoda, Aspidogastrea, Aspidogastridae), a T parasite of Cyprinus carpio Linnaeus, 1758 s. lato (Actinopterygii) and freshwater bivalves in East Asia ⁎ S.G. Sokolova, D.M. Atopkinb,c, , M. Urabed a A.N. Severtsov Institute of Ecology and Evolution of the RAS, Moscow, Russia b Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of the RAS, Vladivostok, Russia c Department of Cell Biology and Genetics, Far Eastern Federal University, Vladivostok, Russia d Department of Ecosystem Studies, School of Environmental Science, University of Shiga Prefecture, Hikone, Japan ARTICLE INFO ABSTRACT Keywords: A detailed morphological description and ribosomal DNA (rDNA) sequence molecular data for Aspidogaster ijimai Morphology from Japan are provided. Morphological analysis, including a description of the cirrus-sac, indicate the con- Aspidogastridae specificity of Japanese and continental East Asian A. ijimai specimens. Analysis of ITS1-5.8S-ITS2 rDNA se- ITS quences of Japanese, Chinese and Russian specimens confirmed the morphological results. Phylogenetic analysis 28S using ITS rDNA sequences confirmed that A. ijimai is a sister species for Aspidogaster chongqingensis. Median- DNA sequences joining network analysis showed an initial molecular differentiation step of Russian specimens from group of Phylogeny Japanese-Chinese samples. Our 28S rDNA results based on maximum likelihood (ML) and Bayesian (BI) phy- logenetic analyses indicated well-supported monophyly of the Aspidogaster conchicola + A. ijimai group, a finding that indicates that these species are congeneric. At the same time, our data demonstrated that the genus Lobatostoma is paraphyletic and the family Aspidogastridae is polyphyletic, results that confirm previous studies. 1. Introduction detailed cirrus and excretory system morphology. Molecular-based phylogenetic analyses, provided by Atopkin and collaborators [6], Aspidogastreans are parasitic flatworms that mainly infect mollusks, confirmed conspecificity of different A. ijimai isolates from Russia and fish and freshwater turtles [1]. These worms are characterised by the China. At the same time, conspecificity of Japanese and continental presence of a longitudinal ventral row of suckers, septa or a ventral East Asian A. ijimai specimens has not proven with molecular data yet. adhesive disc divided into alveoli [2,3]. The life cycle of these parasites Herein we represent the new morphological and molecular data on this is devoid of parthenogenetic stages [4]. species from the type locality with analysis of interrelationships within Aspidogaster ijimai Kawamura, 1915 is one of six species of the genus the Aspidogastridae. Aspidogaster Baer, 1827 reported for East Asia [1,5,6]. This species spread in the Russian Primorye and Khabarovsk Regions [6], Japan 2. Materials and methods [7,8], South Korea [9] and China [10–15]. The first description of A. ijimai was performed for worms from the carp, Cyprinus carpio Lin- 2.1. Sample collection and morphological observation naeus, 1758 s. lato (Actinopterygii), collected from Lake Biwa, west- central Honshu, Japan [7]. Most of later reports about this species were Juvenile (without eggs) and subgravid (with a few eggs) A. ijimai provided for the same host species (reviewed by [1]). However, Zhang specimens were collected from C. carpio s. lato caught in a canal near in 2006 found this parasite in the bivalve clam Corbicula fluminea Lake Biwa or a fishing harbour at Harie in Lake Biwa, Takashima City, (Müller, 1774) [10]. Shiga Prefecture, Japan (35°21′54″N, 136°03′16″E) during December 2 A morphological description of A. ijimai was presented by different and 5, 2016. There are two carp strains in Lake Biwa (Lake Biwa wild authors [7,9–12]. However, these studies contained discrepant data on strain and Eurasian strain), both of which are recognised as almost ⁎ Corresponding author at: Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of the RAS, Vladivostok, Russia. E-mail address: [email protected] (D.M. Atopkin). https://doi.org/10.1016/j.parint.2019.04.017 Received 31 January 2019; Received in revised form 22 March 2019; Accepted 18 April 2019 Available online 20 April 2019 1383-5769/ © 2019 Elsevier B.V. All rights reserved. S.G. Sokolov, et al. Table 1 List of the representatives of the genus Aspidogaster incorporated in analysis of ITS1-5.8S-ITS 2 rDNA sequences (n – number of replicates). Species n Host species Location Author NCBI reg. number Aspidogaster ijimai 12 Cyprinus carpio Linnaeus, 1758 s. lato (Cyprinidae, Lake Biwa, Takashima City, Shiga Prefecture, Japan Original data MK387320–MK387330 Actinopterygii) A. ijimai 1 Id. Khanka Lake, Primorskyi Region, Russia [6] HE866757 A. ijimai 8 Id. Amur River, near Nikolaevsk–na–Amure city, Khabarovsk Region, Russia [6] HE863950– HE863957 A. ijimai 1 Id. Amur River, near Khabarovsk, Khabarovsk Region Russia [6] HE866756 A. ijimai 4 Id. Danjiangkou Reservoir, Danjiangkou, Hubei; Jaingkou Reservoir, Xinyu, Jiangxi; [15] DQ345320–DQ345323 Niushan Lake, Wuhan, Hubei; Jialing River, Beibei, Chongqing, China Aspidogaster chongqingensis 1 Coreius guichenoti (Sauvage et Dabry de Thiersant, Jialing River, Beibei, Chongqing, China [15] (as A. limacoides) DQ345319 1874) (Cyprinidae, Actinopterygii) A. chongqingensis 1 Spinibarbus sinensis (Bleeker, 1871) (Cyprinidae, Jialing River, Beibei, Chongqing, China [15] DQ345324 Actinopterygii) Aspidogaster conchicola 4 Colletopterum anatinum (Linnaeus, 1758) (Unionidae, Tvertza River, Tver Region, Russia [6] HE863959–HE863962 Bivalvia) A. conchicola 4 Cristaria herculea (Middendorff, 1847) (Unionidae, Khanka Lake, Primorskyi Region, Russia [6] HE863958, HE863963–HE863965 Bivalvia) A. conchicola 1 Mylopharyagodon pieus (Richardson, 1846) Danjiangkou Reservoir, Danjiangkou, Hubei; Liangzi Lake, E'zhou, Hubei, China [15] DQ345317, DQ345318 (Cyprinidae, Actinopterygii) Aspidogaster limacoides 4 Rutilus rutilus (Linnaeus, 1758) (Cyprinidae, Rybinsk Reservoir, Yaroslavl Region, Russia [6] HE863966–HE863969 Actinopterygii) A. limacoides 2 Blicca bjoerkna (Linnaeus, 1758) (Cyprinidae, Rybinsk Reservoir, Yaroslavl Region, Russia [6] HE863970–HE863971 Actinopterygii) Outgroup (continued on next page) 168 Table 1 (continued) Species n Host species Location Author NCBI reg. number Multicalyx elegans 1 Callorhinchus milii Bory de Saint-Vincent, Australia: Hobart, Tasmania Gao, Chen and Nie DQ345325 1823 (Callorhinchidae, Chondrichthyes) (unpublished) Parasitology International71(2019)167– 176 S.G. Sokolov, et al. Table 2 List of the representatives of Aspidogastrea incorporated in phylogenetic analysis based on 28S rDNA sequences (n – number of replicates). Species n Host species Location Author NCBI reg. number Aspidogastrea Aspidogaster ijimai (Kawamura, 1915) 3 Cyprinus carpio Linnaeus, 1758 s. lato (Cyprinidae, Actinopterygii) Lake Biwa, Takashima City, Shiga Original data MK387331–MK387333 Prefecture, Japan Aspidogaster conchicola (Baer, 1827) 1 Quadrula pustulosa (Lea, 1831) (Unionidae, Bivalvia) USA [29] AY222162 Cotylaspis sp. 1 Sternotherus odoratus(Latreille, 1801) (Kinosternidae, USA Aymond, Caoili, Tkach and McAllister KM457145 Reptilia) (unpublished) Cotylaspis sp. 1 Pelodiscus sinensis(Wiegmann, 1835) (Trionychidae, Viet Nam [29] AY222165 Reptilia) Cotylogaster basiri (Siddiqi et Cable, 1960) 1 Pogonias cromis(Linnaeus, 1766) (Sciaenidae, Actinopterygii) USA [29] AY222164 Lobatostoma kemostoma (MacCallum et 1 Trachinotus carolinus (Linnaeus, 1766) (Carangidae, Brazil [30] KF561238 169 MacCallum, 1913) Actinopterygii) Lobatostoma manteri (Rohde, 1973) 1 Trachinotus blochii (Lacepède, 1801) (Carangidae, Actinopterygii) Australia [31] AY157177 Multicalyx elegans (Olsson, 1869) 1 Callorhinchus milli Bory de Saint-Vincent, 1823 Australia [29] AY222163 (Callorhinchidae, Chondrichthyes) Multicotyle purvisi (Dawes, 1941) 1 Siebenrockiella crassicollis(Gray, 1831) (Geoemydidae, Malaysia: Malaya [29] AY222166 Reptilia) Neosychnocotyle maggiae Snyder et (Tkach, 1 Id. Australia: Northern Territory [32] EF015578 2007) Rugogaster hydrolagi (Schell, 1973) 1 C. milii Australia [31] AY157176 Sychnocotyle kholo (Ferguson, Cribb et Smales, 1 Carettochelys insculpta Ramsay, 1886 (Carettochelyidae, Reptilia) Australia: Queensland, Ross River [32] EF015579 1999) Outgroup (Digenea) Brachylaima thompsoni (Sinitsin, 1931) 1 Blarina brevicauda (Say, 1823) (Soricidae, Mammalia) Wisconsin, USA [33] AF184262 Leucochloridium perturbatum (Pojmanska, 1969) 1 Turdus merula Linnaeus, 1758 (Turdidae, Aves) Czech Republic [29] AY222169 Leucochloridium paradoxum (Carus, 1833) 1 Succinea sp.(Succineidae, Gastropoda) Leningrad Oblast, Russia [34] KP938187 Zeylanurotrema spearei (Cribb et Barton, 1991) Bufo marinus (Linnaeus, 1758) (Bufonidae, Amphibia) Australia [29] AY222170 Parasitology International71(2019)167– 176 S.G. Sokolov, et al. Parasitology International 71 (2019) 167–176 Fig. 1. Aspidogaster ijimai, whole specimens. A – neotype, ventral view. B – neoparatype, dorsal view. Scale bars 0.5 mm. different biological species [16]. Strain affiliation in fish was not morphological descriptions are in μm (unless otherwise noted). The identified during this study. Six carp individuals (standard length forebody was measured
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