Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-29T00:36:13.559Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphological and molecular data for species of Lecithaster Lühe, 1901 and Hysterolecithoides Yamaguti, 1934 (Digenea: Lecithasteridae) from fish of East Asia and phylogenetic relationships within the Hemiuroidea Looss, 1899

Published online by Cambridge University Press:  26 November 2018

D.M. Atopkin Open the ORCID record for D.M. Atopkin [Opens in a new window] ,
M. Nakao ,
V.V. Besprozvannykh ,
N.D. Ha ,
H.V. Nguyen  and
M. Sasaki
D.M. Atopkin*
Affiliation:
Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of Russian Academy of Sciences, Vladivostok, Russia Department of Cell Biology and Genetics, Far Eastern Federal University, Vladivostok, Russia
M. Nakao
Affiliation:
Department of Parasitology, Asahikawa Medical University, Midorigaoka-Higashi 2-1, Hokkaido 078-8510, Japan
V.V. Besprozvannykh
Affiliation:
Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of Russian Academy of Sciences, Vladivostok, Russia
N.D. Ha
Affiliation:
Institute of Ecology and Biodiversity, Vietnamese Academy of Sciences and Technology, Hanoi, Vietnam
H.V. Nguyen
Affiliation:
Institute of Ecology and Biodiversity, Vietnamese Academy of Sciences and Technology, Hanoi, Vietnam
M. Sasaki
Affiliation:
Department of Parasitology, Asahikawa Medical University, Midorigaoka-Higashi 2-1, Hokkaido 078-8510, Japan
*
Author for correspondence: D.M. Atopkin, Fax.: +7 4232310193 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Four representatives of the genus Lecithaster and one representative of the genus Hysterolecithoides were found during investigation of the trematode fauna of fish species in Vietnamese, Japanese and eastern coastal waters of the Russian Far East. Based on morphometric data, adult trematodes from Vietnamese Strongylura strongylura and Russian Acanthogobius flavimanus were identified as Lecithaster confusus, trematodes from Vietnamese Hemirhamphus marginatus as L. sayori and from osmerid fishes as L. salmonis. Further, a single specimen of Lecithaster sp. and representatives of Hysterolecithoides epinepheli were found in Vietnamese Siganus fuscescens. Morphological and molecular data, including 18S ribosomal DNA (rDNA) V4 fragment, 28S rDNA D1-D3 fragment, internal transcribed spacers (ITS) and a mitochondrial COI gene fragment were analysed for Lecithaster spp. The results revealed that L. sayori and L. salmonis are not synonyms of L. stellatus and L. gibbosus, respectively, but that Hysterolecithoides frontilatus and H. guangdongensis are junior synonyms of H. epinepheli. The 28S-rDNA-based phylogenetic tree of Hemiuroidea showed a distinct position for the genus Lecithaster with internal differentiation into three subclades, including L. confusus, L. sayori and Lecithaster sp. within the first subclade, L. mugilis and L. sudzuhensis within the second subclade and L. salmonis and L. gibbosus within the third subclade. Bayesian phylogenetic reconstructions of Hemiuroidea showed four clades for members of Hemiuridae and Lecithasteridae. The first clade consisted of Hemiuridae representatives and the second clade represented the genus Lecithaster. The third clade included genera Aponurus and Lecithophyllum (Lecithasteridae) and the fourth clade combined members of lecithasterid Quadrifoliovariinae and Hysterolecithinae and hemiurid Opisthadeninae and Bunocotylidae with high statistical support.

Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e14
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, GR and Barker, SC (1998) Inference of phylogeny and taxonomy within the Didymozoidae (Digenea) from the second internal transcribed spacer (ITS2) of ribosomal DNA. Systematic Parasitology 41, 87–94.Google Scholar
Atopkin, DM et al. (2017) Phylogenetic relationships of Hemiuridae (Digenea: Hemiuroidea) with new morphometric and molecular data of Aphanurus mugilis Tang, 1981 (Aphanurinae) from mullet fish of Vietnam. Parasitology International 66, 824–830.Google Scholar
Besprozvannykh, VV et al. (2017) Morphometric and molecular analyses of two digenean species in mugilid fish: Lecithaster mugilis Yamaguti, 1970 from Vietnam and L. sudzuhensis n. sp. from southern Russian Far East. Journal of Helminthology 91, 326–331.Google Scholar
Blair, D, Bray, RA and Baker, SC (1998) Molecules and morphology in phylogenetic studies of the Hemiuroidea (Digenea: Trematoda: Platyhelminthes). Molecular Phylogenetics and Evolution 9, 15–25.Google Scholar
Bray, RA and Cribb, TH (2000) The status of the genera Hysterolecithoides Yamaguti, 1934, Neotheletrum Gibson & Bray, 1979 and Machidatrema León-Règagnon, 1998 (Digenea: Hemiuroidea), including a description of M. leonae n. sp. from Australian waters. Systematic Parasitology 46, 1–22.Google Scholar
Bray, RA, Cribb, TH and Barker, SC (1993) The Hemiuroidea (Digenea) of pomacentrid fishes (Perciformes) from Heron Island, Queensland, Australia. Systematic Parasitology 24, 159–184.Google Scholar
Calhoun, DM et al. (2013) Hirudinella ventricosa (Pallas, 1774) Baird, 1853 represents a species complex based on ribosomal DNA. Systematic Parasitology 86, 197–208.Google Scholar
Carreras-Aubets, M et al. (2011) A new cryptic species of Aponurus Looss, 1907 (Digenea: Lecithasteridae) from Mediterranean goatfish (Teleostei: Mullidae). Systematic Parasitology 79, 145–159.Google Scholar
Chambers, CB and Cribb, TH (2006) Phylogeny, evolution and biogeography of the Quadrifoliovariinae Yamaguti, 1965 (Digenea: Lecithasteridae). Systematic Parasitology 63, 61–82.Google Scholar
Claxton, AT et al. (2017) Parasites of the vermilion snapper, Rhomboplites aurorubens (Cuvier), from the western Atlantic Ocean. Comparative Parasitology 84, 1–14.Google Scholar
Cribb, TH et al. (2001) Relationships of the Digenea – evidence from molecules and morphology. In Littlewood, DTJ and Bray, RA (Eds), Interrelationships of Platyhelminthes. London: Taylor & Francis, pp. 186–193.Google Scholar
Darriba, D et al. (2012) jModeltest2: more models, new heuristics and parallel computing. Nature Methods 9, 772.Google Scholar
Faltýnková, A et al. (2017) Biodiversity and evolution of digeneans of fishes in the Southern Ocean. In Klimpel, S, Heinz, T and Mehlhorn, K (Eds), Biodiversity and Evolution of Parasitic Life in the Southern Ocean. Switzerland: Springer International Publishing, pp. 49–75.Google Scholar
Gibson, DI (2002) Famali Lecithasteridae Odhner, 1905. In Gibson, DI, Jones, A and Bray, RA (Eds), Keys to the Trematoda, Vol. 2. Wallingford: CAB International, pp. 381–396.Google Scholar
Huelsenbeck, JP et al. (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294, 2310–2314.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0. Molecular Biology and Evolution 33, 1870–1874.Google Scholar
León-Règagnon, V (1998) Machidatrema n. gen. (Digenea: Hemiuridae: Bunocotylinae) and phylogenetic analysis of its species. Journal of Parasitology 84, 140–146.Google Scholar
León-Règagnon, V, Pérez-Ponce de León, G and Brooks, DR (1998) Phylogenetic analysis of the Bunocotylinae Dollfus, 1950 (Digenea: Hemiuridae). Journal of Parasitology 84, 147–152.Google 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, pp. 262–278.Google Scholar
Liu, S et al. (2010) Digenean parasites of Chinese marine fishes: a list of species, hosts and geographical distribution. Systematic Parasitology 75, 1–52.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, 323–327.Google Scholar
Machida, M (2003) Additional two species of digenean trematodes from mullet of Southern Japan. Bulletin of Natural Science Museum 29, 125–129.Google Scholar
Manter, HW (1969) Some digenetic trematodes of marine fishes of New Caledonia. Part IV. Hemiuridae and summary. Proceedings of the Helminthological Society of Washington 36, 194–204.Google Scholar
Manter, HW and Pritchard, MH (1960) Additional hemiurid trematodes from Hawaiian fishes. Proceedings of the Helminthological Society of Washington 27, 165–180.Google Scholar
Margolis, L and Boyce, NP (1969) Life span, maturation, and growth of two hemiurid trematodes, Tubulovesicula lindbergi and Lecithaster gibbosus, in Pacific salmon (genus Oncorhynchus). Journal of the Fisheries Research Board of Canada 26, 893–907.Google Scholar
Marzoug, D et al. (2014) A new species of Saturnius Manter, 1969 (Digenea: Hemiuridae) from Mediterranean mullet (Teleostei: Mugilidae). Systematic Parasitology 87, 127–134.Google Scholar
Olmo, AP et al. (2006) Description of Wardula bartolii n.sp. (Digenea: Mesometridae) and three newly recorded accidental parasites of Boops boops L. (Sparidae) in the NE Atlantic. Systematic Parasitology 63, 99–109.Google Scholar
Olson, PD et al. (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733–755.Google Scholar
Overstreet, RM (1973) Some species of Lecithaster Lühe, 1901 (Digenea: Hemiuridae) and related genera from fishes in the Northern Gulf of Mexico. Transactions of the American Microscopical Society 92, 231–240Google Scholar
Pan, JP (1984) Two new genera and three new species of hemiurid and Maseniidae from from Kwangtung fishes. In Institute of Hydrobiology Academia Sinica (Ed.), Parasitic Organisms of Freshwater Fish of China. Beijing: Agricultural Publishing House, pp. 125–132 (in Chinese).Google Scholar
Pankov, P et al. (2006) Robinia aurata n.g., n. sp. (Digenea: Hemiuridae) from the mugilid Liza aurata with a molecular confirmation of its position within the Hemiuroidea. Journal of Parasitology 133, 217–227.Google Scholar
Pérez-del Olmo, A et al. (2006) Descriptions of Wardula bartolii n. sp. (Digenea: Mesometridae) and three newly recorded accidental parasites of Boops boops L. (Sparidae) in the NE Atlantic. Systematic Parasitology 63, 97–107.Google Scholar
Schrandt, MN et al. (2016) Novel infection site and ecology of cryptic Didymocystis sp. (Trematoda) in the fish Scomberomorus maculatus. Journal of Parasitology 102, 297–305.Google Scholar
Shen, JW and Qiu, ZZ (1995) Studies on the Trematodes of Fishes from Yellow Sea and the Bo Hai Sea. Beijing: Science Press (in Chinese).Google Scholar
Skrjabin, KI (1954) Family Lecithasteridae Skrjabin et Guschanskaya, 1954. In Skrjabin, KI (Ed.) Trematodes of Animals and Man. Principles of Trematodology. Moscow: Akademiya Nauk Press, pp. 511–599 (in Russian).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, 191–202.Google Scholar
Sokolov, SG et al. (2018a) 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, 74–78.Google Scholar
Sokolov, SG et al. (2018b) Phylogenetic analysis of the superfamily Hemiuroidea (Platyhelminthes, Neodermata: Trematoda) based on partial 28S rDNA sequences. Parasitology, in press. doi: 10.1017/S0031182018001941.Google Scholar
Tkach, VV et al. (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56, 1–15.Google Scholar
Truett, GE (2006) Preparation of genomic DNA from animal tissues. In Kieleczawa, J (Ed.), The DNA Book: Protocols and Procedures for the Modern Molecular Biology. Sudbury, MA: Jones & Bartlett Publisher, pp. 33–46.Google Scholar
WoRMS Editorial Board (2014) World Register of Marine Species. Available at http://www.marinespecies.org (accessed March 2014).Google Scholar
Yamaguti, S (1934) Studies on the helminth fauna of Japan. Part 2. Trematodes of fishes, I. Japanese Journal of Zoology 5, 249–541.Google Scholar
Yamaguti, S (1938) Studies on the helminth fauna of Japan. Part 21. Trematodes of fishes, IV. Japanese Journal of Zoology 8, 128–130.Google Scholar
Yamaguti, S (1940) Studies on the helminth fauna of Japan. Part 21. Trematodes of fishes. VII. Japanese Journal of Zoology 9, 35–108.Google Scholar
Yamaguti, S (1953) Parasitic worms mainly from celebs. Part 3. Digenetic trematodes of fishes, II. Acta Medica Okayama 8, 1–45.Google Scholar
Yamaguti, S (1970) Digenetic Trematodes of Hawaiian Fishes. Tokyo: Keigaku Publishing Co.Google Scholar