Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-25T14:12:35.197Z Has data issue: false hasContentIssue false

Diversity of European lissorchiid trematodes from fish and snail hosts with comments on the validity of the genus Parasymphylodora Szidat, 1943

Published online by Cambridge University Press:  14 September 2022

R. Petkevičiūtė*
Affiliation:
Institute of Ecology of Nature Research Centre, Akademijos 2, LT-08412 Vilnius, Lithuania
V. Stunžėnas
Affiliation:
Institute of Ecology of Nature Research Centre, Akademijos 2, LT-08412 Vilnius, Lithuania
G. Stanevičiūtė
Affiliation:
Institute of Ecology of Nature Research Centre, Akademijos 2, LT-08412 Vilnius, Lithuania
*
Author for correspondence: Romualda Petkevičiūtė, E-mail: [email protected]

Abstract

Genetic markers, DNA sequences and karyotypes, of some European lissorchiid species from their intermediate and final hosts were obtained to clarify controversial data about their life cycles and taxonomy, and to reveal phylogenetic affinities. The life cycles of three species have been confirmed for the first time based on molecular data. Comparative analysis of internal transcribed spacer 2 (ITS2) and partial 28S rDNA sequences has undoubtedly proven that cercariaeum of type-species of the genus Asymphylodora, Asymphylodora tincae, develops in pulmonate snails, Anisus vortex and Stagnicola palustris, but not in the genus Bithynia. The faucet snail, Bithynia tentaculata, serves as the first intermediate host for Parasymphylodora (=Asymphylodora) markewitschi and Parasymphylodora parasquamosa; adults of both species were isolated from the common rudd, Scardinius erythrophthalmus. It has also been confirmed that B. tentaculata serves as the second intermediate host for P. parasquamosa. Phylogenetic analysis supports the validity of the genus Parasymphylodora. Two species, Parasymphylodora markewitschi and P. parasquamosa, with cercariaeum belonging to the Parasquamosum group, are closely related and are being recovered as a well-defined evolutionary lineage in phylogenetic trees. A significant divergence between Parasymphylodora spp. and Asymphylodora spp. was revealed. The diploid chromosome set of P. markewitschi is composed of 14 chromosomes and does not show similarities with karyotypes of other lissorchiid species. Asymphylodora progenetica and Asymphylodora tincae share the basal diploid value of the family, 2n = 20, and reveal very close morphology of the corresponding chromosome pairs. Karyotypic similarities of these species are in accordance with molecular phylogenetic data. Thus, the available molecular and cytogenetic data support the assignment of P. markewitschi and P. parasquamosa to a separate genus, meanwhile, the assignment of A. progenetica to the genus Parasymphylodora was not justified.

Type
Research Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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

Baker, RB and Bickham, JW (1980) Karyotypic evolution in bats: evidence of extensive and conservative chromosomal evolution in closely related taxa. Systematic Zoology 29(3), 239253.CrossRefGoogle Scholar
Baker, RB and Bickham, JW (1986) Speciation by monobrachial centric fusions. The Proceedings of the National Academy of Sciences of the United states of America 83(21), 82458248.Google ScholarPubMed
Baršienė, J (1993) The karyotypes of trematodes. Vilnius, Academia. [In Russian.]Google ScholarPubMed
Baršienė, J, Roca, V, Tapia, G and Martin, JE (1995) Chromosome analysis of two digenean species of the families Heterophyidae and Monorchiidae (Trematoda). Research and Reviews in Parasitology 55(3), 149154.Google Scholar
Besprozvannykh, VV (2005) Life cycles of the trematode Parasymphilodora japonica (Yamaguti, 1938) and P. markewitschi (Kulakowskaja, 1947) (Monorchidae) in the conditions of Primore land. Parazitologiya 39(2), 137145. [In Russian.]Google Scholar
Besprozvannykh, VV, Ermolenko, AV and Atopkin, DM (2012) The life cycle of Asymphylodora perccotti sp. n. (Trematoda: Lissorchiidae) in the Russian Southern Far East. Parasitology International 61(2), 235241.Google Scholar
Bowles, J, Blair, D and McManus, DP (1995) A molecular phylogeny of the human schistosomes. Molecular Phylogenetic and Evolution 4(2), 103109.CrossRefGoogle ScholarPubMed
Bray, RA (2008) Family Lissorchiidae Magath, 1917. pp. 177186. In Jones, A, Gibson, DI, and Bray, RA (Eds) Keys to the Trematoda, Vol. 3. Wallingford, CABI.Google Scholar
Bykhovskaya-Pavlovskaya, IE and Kulakova, AP (1971) Cercariae from Bithynia (Bithynia tentaculata and B. leachii) in Curonian Lagoon. Parazitologiya 5(3), 222232. [In Russian.]Google Scholar
Bykhovskaya-Pavlovskaya, IE and Kulakova, AP (1987) Trematoda. pp. 77198. In Bauer, ON (Ed.) Key to parasites of freshwater fish of USSR, Vol. 3. Leningrad, Nauka. [In Russian.]Google Scholar
Chernogorenko, MI (1983) Larvae of trematodes in molluscs in Dnepr River and its reservoirs (fauna, biology and peculiarities of formation). p. 212. Kiev, Naukova Dumka. [In Russian.]Google Scholar
Cichy, A, Faltýnková, A and Żbikowska, E (2011) Cercariae (Trematoda, Digenea) in European freshwater snails – a checklist of records from over one hundred years. Folia Malacologica 19(3), 165189.CrossRefGoogle Scholar
Claxton, AT, Fuehring, AD, Andres, MJ, Moncrief, TD and Curran, SS (2017) Parasites of the Vermilion Snapper, Rhomboplites aurorubens (Cuvier), from the Western Atlantic Ocean. Comparative Parasitology 84(1), 114.CrossRefGoogle Scholar
Cribb, TH (2016) Editorial: The biodiversity of trematodes of fishes. Systematic Parasitology 93(3), 219221.CrossRefGoogle ScholarPubMed
Cribb, TH and Bray, RA (2010) Gut wash, body soak, blender and heat-fixation: approaches to the effective collection, fixation and preservation of trematodes of fishes. Systematic Parasitology 76(1), 17.CrossRefGoogle Scholar
Cribb, TH, Anderson, GR, Adlard, RD and Bray, RA (1998) A DNA-based demonstration of a three-host life-cycle for the Bivesiculidae (Platyhelminthes: Digenea). International Journal for Parasitology 28(11), 17911795.CrossRefGoogle Scholar
Cribb, TH, Wee, NQX, Bray, RA and Cutmore, SC (2018) Monorchis lewisi n. sp. (Trematoda: Monorchiidae) from the surf bream, Acanthopagrus australis (Sparidae), in Moreton Bay, Australia. Journal of Helminthology 92(1), 100108.CrossRefGoogle Scholar
Curran, SS, Tkach, VV and Overstreet, RM (2006) A review of Polylekithum Arnold, 1934 and its familial affinities using morphological and molecular data, with description of Polylekithum catahoulensis sp. nov. Acta Parasitologica 51(4), 238248.CrossRefGoogle Scholar
Cutmore, SC, Miller, TL, Curran, SS, Bennett, MB and Cribb, TH (2013) Phylogenetic relationships of the Gorgoderidae (Platyhelminthes: Trematoda), including the proposal of a new subfamily (Degeneriinae n. subfam.). Parasitology Research 112(8), 30633074.CrossRefGoogle Scholar
Dubois, G (1929) Les cercaires de la région de Neuchâtel [Cercariae from the Neuchâtel region]. Bulletin de la Société Neuchateloise des Sciences Naturelles 53(1), 1177. [In French.]Google Scholar
Faltýnková, A, Sures, B and Kostadinova, A (2016) Biodiversity of trematodes in their intermediate mollusc and fish hosts in the freshwater ecosystems of Europe. Systematic Parasitology 93(3), 283293.CrossRefGoogle ScholarPubMed
Grossman, AI, Short, RB and Cain, GD (1981) Karyotype evolution and sex chromosome differentiation in schistosomes (Trematoda, Schistosomatidae). Chromosoma 84(3), 413430.CrossRefGoogle Scholar
Khan, D (1962) Two new species of cercariaea from London (U.K.). Zeitschrift für Parasitenkunde 21(1), 195201.CrossRefGoogle Scholar
Kudlai, OS (2010) The first record of Asympylodora progenetica (Trematoda, Monorchiidae) in Ukraine. Vestnik Zoologii 44(6), 559562.Google Scholar
Kulakova, AP (1972) A new species of the genus Parasymphylodora (Trematoda, Monorchiidae) and its larva. Parazitologiya 6(2), 137142. [In Russian.]Google ScholarPubMed
Kulakova, AP (1982) New data on Asymphylodora progenetica = Parasymphylodora progenetica (Trematoda, Monorchiidae). Parazitologiya 16(1), 7881. [In Russian.]Google Scholar
Lambert, M (1976) Cycle biologique de Parasymphylodora markewitschi (Kulakowskaja, 1947) (Trematoda, Digenea, Monorchiidae) [Life cycle of Parasymphylodora markewitschi (Kulakowskaja, 1947) (Trematoda, Digenea, Monorchiidae)]. Bulletin du Muséum National d'Histoire Naturelle. Zoologie 284(407), 11071114.Google Scholar
Levan, A, Fredga, K and Sandberg, A (1964) Nomenclature for centromere position on chromosomes. Hereditas 52(2), 201220.CrossRefGoogle Scholar
Méndez, J, Insua, A and López-Piñón, MJ (2001) Caracterización citogenética en moluscos bivalvos [Cytogenetic characterization in bivalve molluscs]. pp. 1548. In Méndez, J (Ed.) Los moluscos bivalvos: Aspectos citogenéticos, moleculares y aplicados [Bivalve molluscs: cytogenetic, molecular and applied aspects], Universidade da Coruña, A Coruña, Galicia. Servicio de publicacións. [In Spanish.]Google Scholar
Morley, NJ, Adam, ME and Lewis, JW (2004) The role of Bithynia tentaculata in the transmission of larval digeneans from a gravel pit in the Lower Thames Valley. Journal of Helminthology 78(2), 129135.CrossRefGoogle ScholarPubMed
Našincová, V and Scholz, T (1994) The life cycle of Asymphylodora tincae (Modeer 1790) (Trematoda: Monorchiidae): a unique development in monorchiid trematodes. Parasitology Research 80(3), 192197.CrossRefGoogle ScholarPubMed
Niewiadomska, K (2003) Pasożyty ryb Polski. Przywry – Digenea [Polish fish parasites. Flukes–Digenea]. 169 pp. Warszawa, Polskie Towarzystwo Parazytologiczne. [In Polish.]Google Scholar
Nur, U (1989) Reproductive biology and genetics. Chromosomes, sex-ratios, and sex determination. pp. 179190. In Rosen, D (Ed.) Armoured scale insects, their biology, natural enemies and control, Vol. A. Amsterdam, Elsevier Science Publishers.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(7), 733755.CrossRefGoogle Scholar
Petkevičiūtė, R and Stanevičiūtė, G (2008) Comparative karyological analysis of three members of Allocreadiidae (Digenea): taxonomic and phylogenetic implications. Parasitology Research 103(5), 11051110.CrossRefGoogle ScholarPubMed
Petkevičiūtė, R, Stunžėnas, V and Stanevičiūtė, G (2012) Clarification of the systematic position of Cercariaeum crassum Wesenberg-Lund, 1934 (Digenea), based on karyological analysis and DNA sequences. Journal of Helminthology 86(3), 293301.Google Scholar
Petkevičiūtė, R, Stunžėnas, V and Stanevičiūtė, G (2014) Differentiation of European freshwater bucephalids (Digenea: Bucephalidae) based on karyotypes and DNA sequences. Systematic Parasitology 87(2), 199212.CrossRefGoogle ScholarPubMed
Petkevičiūtė, R, Kudlai, O, Stunžėnas, V and Stanevičiūtė, G (2015) Molecular and karyological identification and morphological description of cystocercous cercariae of Phyllodistomum umblae and Phyllodistomum folium (Digenea, Gorgoderidae) developing in European sphaeriid bivalves. Parasitology International 64(5), 441447.CrossRefGoogle ScholarPubMed
Petkevičiūtė, R, Stanevičiūtė, G and Stunžėnas, V (2020) Exploring species diversity of lissorchiid trematodes (Digenea: Lissorchiidae) associated with the gravel snail, Lithoglyphus naticoides, in European freshwaters. Journal of Helminthology 94, e152, 1–10.CrossRefGoogle ScholarPubMed
Posada, D (2008) jModelTest: phylogenetic modelling averaging. Molecular Biology and Evolution 25(7), 12531256.CrossRefGoogle Scholar
Rao, NP and Rai, KS (1987) Inter and intraspecific variation in nuclear DNA content in Aedes mosquitoes. Heredity 59(2), 253258.CrossRefGoogle ScholarPubMed
Scholz, T, De Chambrier, A, Kuchta, R, Littlewood, DTJ and Waeschenbach, A (2013) Macrobothriotaenia ficta (Cestoda: Proteocephalidea), a parasite of sunbeam snake (Xenopeltis unicolor): Example of convergent evolution. Zootaxa 3640(3), 485499.CrossRefGoogle ScholarPubMed
Scholz, T, Besprozvannykh, VV, Boutorina, TE, et al. (2016) Trematode diversity in freshwater fishes of the Globe I: ‘Old World’. Systematic Parasitology 93(3), 257269.CrossRefGoogle ScholarPubMed
Serbina, EA (2010) Coevolution of the host – parasite systems (Bithyniidae-Trematode). pp. 239259. In Be′er, SA (Ed.) Biodiversity and ecology of parasites, Vol. 46. Transactions of Center for Parasitology. Nauka, Moscow. [In Russian.]Google Scholar
Serbina, EA (2014) Larval trematodes in bithyniid snails (Gastropoda: Bithyniidae) in the lake-rivers systems from the steppe zone (The West Siberian Plain, Russia). Helminthologia 51(4), 293300.CrossRefGoogle Scholar
Serkova, OP and Bychovsky, BE (1940) Asymphylodora progenetica n. sp. with some information on its morphology and life-cycle. Parazitologicheskij Sbornik 8(1), 162175. [In Russian.]Google Scholar
Shimazu, T (1992) Trematodes of the genera Asymphylodora, Anapalaeorchis and Palaeorchis (Digenea: Lissorchiidae) from freshwater fishes of Japan. Journal of Nagano Prefectural College 47(1), 119.Google Scholar
Shimazu, T (2016) Digeneans parasitic in freshwater fishes (Osteichthyes) of Japan. VI. Lissorchiidae. Bulletin of the National Museum of Nature and Science, Series B 42(1), 122.Google Scholar
Sobolev, AA (1955) Family Monorchidae Odhner, 1911. pp. 257464. In Skriabin, KI (Ed.) Trematodes of animals and Man. Essentials of trematodology, Vol XI. Publishing House of the AN SSSR, Moscow. [In Russian.]Google Scholar
Sokolov, SG and Gordeev, II (2019) Asaccotrema vietnamiense n. gen.; n. sp. (Trematoda: Monorchioidea), a new aberrant representative of lissorchiid trematodes from the sidestripe rasbora, Rasbora paviana Tirant (Actinopterygii: Cyprinidae), Vietnam. Zootaxa 4674(4), 26.CrossRefGoogle Scholar
Sokolov, SG, Voropaeva, EL and Atopkin, DM (2020) A new species of deropristid trematode from the sterlet Acipenser ruthenus (Actinopterygii: Acipenseridae) and revision of superfamily affiliation of the family Deropristidae. Zoological Journal of the Linnean Society 190(2), 448459.CrossRefGoogle Scholar
Stunkard, HW (1959) The morphology and life-history of the digenetic trematode, Asymphylodora amnicolae n.sp; the possible significance of progenesis for the phylogeny of the Digenea. Biological Bulletin 117(3), 562581.CrossRefGoogle Scholar
Stunžėnas, V, Petkevičiūtė, R and Stanevičiūtė, G (2011) Phylogeny of Sphaerium solidum (Bivalvia) based on karyotype and sequences of 16S and ITS1 rDNA. Central European Journal of Biology 6(1), 105117.Google Scholar
Stunžėnas, V, Petkevičiūtė, R, Poddubnaya, LG, Stanevičiūtė, G and Zhokhov, AE (2017) Host specificity, molecular phylogeny and morphological differences of Phyllodistomum pseudofolium Nybelin, 1926 and Phyllodistomum angulatum Linstow, 1907 (Trematoda: Gorgoderidae) with notes on Eurasian ruffe as final host for Phyllodistomum spp. Parasites & Vectors 10, 286.CrossRefGoogle ScholarPubMed
Szidat, L (1943) Die Fischtrematoden der Gattung Asymphylodora Looss, 1899 und Verwandte [The fish trematodes of the genus Asymphylodora Looss, 1899 and relatives]. Zeitschrift für Parasitenkunde 13(1), 2561. [In German.]CrossRefGoogle Scholar
Tamura, K, Stecher, G and Kumar, S (2021) MEGA11: Molecular Evolutionary Genetics Analysis version 11. Molecular Biology and Evolution 38(7), 30223027.CrossRefGoogle ScholarPubMed
Thompson, JD, Higgins, DG and Gibson, TJ (1994) CLUSTAL w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22(22), 46734680.CrossRefGoogle ScholarPubMed
Tkach, V, Grabda-Kazubska, B, Pawlowski, J and Swiderski, Z (1999) Molecular and morphological evidences for close phylogenetic affinities of the genera Macrodera, Leptophallus, Metaleptophallus, and Paralepoderma (Digenea, Plagiorchioidea). Acta Parasitologica 44(3), 170179.Google Scholar
Tkach, VV, Pavlowski, J, Mariaux, J and Swiderski, Z (2001) Molecular phylogeny of the suborder Plagiorchiata and its position in the system of Digenea. pp. 186193. In Littlewood, DTJ and Bray, RA (Eds) Interrelationships of the platyhelminthes. London, Taylor and Francis.Google Scholar
Tkach, VV, Littlewood, DTJ, Olson, PD, Kinsella, MJ and Swiderski, Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56(1), 115.CrossRefGoogle Scholar
Truong, TN, Warren, MB, Ksepka, SP, Curran, SS and Bullard, SA (2021) Posthovitellinum psiloterminae n. gen., n. sp. (Digenea: Lissorchiidae) infecting the intestine of Cyclocheilos enoplos (Cypriniformes: Cyprinidae) in the Mekong River, Vietnam. Journal of Parasitology 107(3), 431445.CrossRefGoogle Scholar
Van den Broek, E and de Jong, N (1979) Studies on the life cycle of Asymphylodora tincae (Modeer, 1790) (Trematoda: Monorchiidae) in a small lake near Amsterdam. Part 1. The morphology of various stages. Journal of Helminthology 53(1), 7989.CrossRefGoogle Scholar
Wee, NQX, Cutmore, SC and Cribb, TH (2019) Four new monorchiids from the golden trevally, Gnathanodon speciosus (Forsskål) (Perciformes: Carangidae), in Moreton Bay, Australia. Systematic Parasitology 96(3), 265–278.CrossRefGoogle Scholar
White, MJD (1978) Chain processes in chromosomal speciation. Systematic Zoology 27(3), 285298.CrossRefGoogle Scholar
Zietse, MA, Van Den Broek, E and Erwteman-Ooms, EEA (1981) Studies on the life-cycle of Asymphylodora tincae (Modeer, 1790) (Trematoda: Monorchiidae) in a small lake near Amsterdam: Part 2: The relations between Asymphylodora tincae and its definitive host, Tinca tinca. Journal of Helminthology 55, 239246.CrossRefGoogle Scholar