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Another plea for ‘best practice’ in molecular approaches to trematode systematics: Diplostomum sp. clade Q identified as Diplostomum baeri Dubois, 1937 in Europe

Published online by Cambridge University Press:  07 January 2022

Anna Faltýnková ,
Olena Kudlai Open the ORCID record for Olena Kudlai [Opens in a new window] ,
Camila Pantoja ,
Galina Yakovleva  and
Daria Lebedeva
Anna Faltýnková
Affiliation:
Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05 České Budějovice, Czech Republic Department of Forest Ecology, Faculty of Forestry and Wood Technology, Mendel University in Brno, Zemědělská 3, Brno 613 00, Czech Republic
Olena Kudlai*
Affiliation:
Institute of Ecology, Nature Research Centre, Akademijos 2, 08412 Vilnius, Lithuania
Camila Pantoja
Affiliation:
Institute of Ecology, Nature Research Centre, Akademijos 2, 08412 Vilnius, Lithuania
Galina Yakovleva
Affiliation:
Institute of Biology, Karelian Research Center, Russian Academy of Sciences, Pushkinskaya St. 11, 185910 Petrozavodsk, Russia
Daria Lebedeva
Affiliation:
Institute of Biology, Karelian Research Center, Russian Academy of Sciences, Pushkinskaya St. 11, 185910 Petrozavodsk, Russia
*
Author for correspondence: Olena Kudlai, E-mail: olena.kudlai@gmail.com
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Abstract

DNA sequence data became an integral part of species characterization and identification. Still, specimens associated with a particular DNA sequence must be identified by the use of traditional morphology-based analysis and correct linking of sequence and identification must be ensured. Only a small part of DNA sequences of the genus Diplostomum (Diplostomidae) is based on adult isolates which are essential for accurate identification. In this study, we provide species identification with an aid of morphological and molecular (cox1, ITS-5.8S-ITS2 and 28S) characterization of adults of Diplostomum baeri Dubois, 1937 from naturally infected Larus canus Linnaeus in Karelia, Russia. Furthermore, we reveal that the DNA sequences of our isolates of D. baeri are identical with those of the lineage Diplostomum sp. clade Q , while other sequences labelled as the ‘D. baeri’ complex do not represent lineages of D. baeri. Our new material of cercariae from Radix balthica (Linnaeus) in Ireland is also linked to Diplostomum sp. clade Q. We reveal that D. baeri is widely distributed in Europe; as first intermediate hosts lymnaeid snails (Radix auricularia (Linnaeus), R. balthica) are used; metacercariae occur in eye lens of cyprinid fishes. In light of the convoluted taxonomy of D. baeri and other Diplostomum spp., we extend the recommendations of Blasco-Costa et al. (2016, Systematic Parasitology 93, 295–306) for the ‘best practice’ in molecular approaches to trematode systematics. The current study is another step in elucidating the species spectrum of Diplostomum based on integrative taxonomy with well-described morphology of adults linked to sequences.

Keywords

IrelandLaridaeLymnaeidaenuclear and mitochondrial DNARussiatrematoda
Type
Research Article
Information
Parasitology , Volume 149 , Issue 4 , April 2022 , pp. 503 - 518
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Achatz, TJ, Martens, JR, Kostadinova, A, Pulis, EE, Orlofske, SA, Bell, JA, Fecchio, A, Oyarzún-Ruiz, P, Syrota, YY and Tkach, VV (2021) Molecular phylogeny of Diplostomum, Tylodelphys, Austrodiplostomum and Paralaria (Digenea: Diplostomidae) necessitates systematic changes and reveals a history of evolutionary host switching events. International Journal for Parasitology (in press). doi: 10.1016/j.ijpara.2021.06.002Google ScholarPubMed
Aksenova, OV, Bolotov, IN, Gofarov, M, Kondakov, AV, Vinarski, MV, Bespalaya, Y, Kolosova, Y, Palatov, DM, Sokolova, SE, Spitsyn, VM, Tomilova, AA, Travina, OV and Vikhrev, IV (2018) Species richness, molecular taxonomy and biogeography of the radicine pond snails (Gastropoda: Lymnaeidae) in the Old World. Scientific Reports 8, 11199.CrossRefGoogle ScholarPubMed
Antar, R, Georgieva, S, Gargouri, L and Kostadinova, A (2015) Molecular evidence for the existence of species complexes within Macvicaria Gibson & Bray, 1982 (Digenea: Opecoelidae) in the western Mediterranean, with descriptions of two new species. Systematic Parasitology 91, 211–229.CrossRefGoogle ScholarPubMed
Behrmann-Godel, J (2013) Parasite identification, succession and infection pathways in perch fry (Perca fluviatilis): new insights through a combined morphological and genetic approach. Parasitology 140, 509–520.CrossRefGoogle ScholarPubMed
Bensch, S, Inumaru, M, Sato, Y, Lee Cruz, L, Cunningham, AA, Goodman, SJ, Levin, II, Parker, PG, Casanueva, P, Hernández, MA, Moreno-Rueda, G and Rojo, MA (2021) Contaminations contaminate common databases. Molecular Ecology Resources 21, 355–362.CrossRefGoogle ScholarPubMed
Blasco-Costa, I and Locke, SA (2017) Life history, systematics and evolution of the Diplostomoidea Poirier, 1886: progress, promises and challenges emerging from molecular studies. In Rollinson, D and Stothard, JR (eds), Advances in Parasitology, Vol. 98. UK: London: Academic Press, pp. 167–225.Google Scholar
Blasco-Costa, I, Faltýnková, A, Georgieva, S, Skírnisson, K, Scholz, T and Kostadinova, A (2014) Fish pathogens near the Arctic circle: molecular, morphological and ecological evidence for unexpected diversity of Diplostomum (Digenea: Diplostomidae) in Iceland. International Journal for Parasitology 44, 703–715.CrossRefGoogle Scholar
Blasco-Costa, I, Cutmore, SC, Miller, TL and Nolan, MJ (2016) Molecular approaches to trematode systematics: ‘best practice’ and implications for future study. Systematic Parasitology 93, 295–306.CrossRefGoogle ScholarPubMed
Bridge, PD, Roberts, PJ, Spooner, BM and Panchal, G (2003) On the unreliability of published DNA sequences. New Phytologist 160, 43–48.CrossRefGoogle ScholarPubMed
Cort, WW and Brackett, S (1937) A new strigeid cercaria which produces a bloat disease in tadpoles. Journal of Parasitology 23(Suppl.), S563–S564.Google Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772–772.CrossRefGoogle ScholarPubMed
Dubinina, MN (1971) Parasitological Study of Birds. Leningrad: Nauka (in Russian).Google Scholar
Dubois, G (1937) Sur quelques strigéidés. Notes préliminaires. Revue Suisse de Zoologie 44, 391–396.CrossRefGoogle Scholar
Dubois, G (1938) Monographie des Strigeida (Trematoda). Mémoires de la Société des Sciences Naturelles de Cherbourg 6, 1–535.Google Scholar
Dubois, G (1970) Synopsis des Strigeidae et des Diplostomatidae (Trematoda). Mémoires de la Société des Sciences Naturelles de Cherbourg 10, 259–727.Google Scholar
Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.CrossRefGoogle ScholarPubMed
Galazzo, DE, Dayanandan, S, Marcogliese, DJ and McLaughlin, JD (2002) Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA-sequence data and comparisons with European congeners. Canadian Journal of Zoology 80, 2207–2217.CrossRefGoogle Scholar
Georgieva, S, Soldánová, M, Pérez-del-Olmo, A, Dangel, RD, Sitko, J, Sures, B and Kostadinova, A (2013) Molecular prospecting for European Diplostomum (Digenea: Diplostomidae) reveals cryptic diversity. International Journal for Parasitology 43, 57–72.CrossRefGoogle ScholarPubMed
Guindon, S, Dufayard, JF, Lefort, V, Anisimova, M, Hordijk, W and Gascuel, O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.CrossRefGoogle ScholarPubMed
Heneberg, P, Sitko, J and Těšínský, M (2020) Paraphyly of Conodiplostomum Dubois, 1937. Parasitology International 76, 102033.CrossRefGoogle ScholarPubMed
Hey, J, Waples, RS, Arnold, ML, Butlin, RK and Harrison, RG (2003) Understanding and confronting species uncertainty in biology and conservation. Trends in Ecology and Evolution 18, 97–603.CrossRefGoogle Scholar
Hoogendoorn, C, Smit, NJ and Kudlai, O (2020) Resolution of the identity of three species of Diplostomum (Digenea: Diplostomidae) parasitising freshwater fishes in South Africa, combining molecular and morphological evidence. International Journal for Parasitology: Parasites and Wildlife 11, 50–61.Google ScholarPubMed
Karvonen, A and Marcogliese, DJ (2020) Diplostomiasis (Diplostomum spathaceum and related species). In Woo, PTK, Leong, J-A and Buchmann, K (eds), Climate Change and Infectious Fish Diseases. Wallingford: CABI, pp. 434–456.CrossRefGoogle Scholar
Karvonen, A, Seppälä, O and Valtonen, ET (2004) Eye-fluke induced cataract formation in fish: quantitative analysis using and ophthalmological microscope. Parasitology 129, 473–478.CrossRefGoogle ScholarPubMed
Kudlai, O, Oros, M, Kostadinova, A and Georgieva, S (2017) Exploring the diversity of Diplostomum (Digenea: Diplostomidae) in fishes from the river Danube using DNA mitochondrial barcodes. Parasites & Vectors 10, 592.CrossRefGoogle Scholar
Landeryou, T, Ropiquet, A, Kett, SM, Wildeboer, D and Lawton, SP (2020) Characterization of the complete mitochondrial genome of Diplostomum baeri. Parasitology International 79, 102166.CrossRefGoogle ScholarPubMed
Lebedeva, DI, Chrisanfova, GG, Ieshko, EP, Guliaev, AS, Yakovleva, GA, Mendsaikhan, B and Semyenova, SK (2021) Morphological and molecular differentiation of Diplostomum spp. metacercariae from brain of minnows (Phoxinus phoxinus L.) in four populations of northern Europe and East Asia. Infection, Genetics and Evolution 92, 104911.CrossRefGoogle ScholarPubMed
Littlewood, DT, Rohde, K and Clough, KA (1997) Parasite speciation within or between host species? – Phylogenetic evidence from site-specific polystome monogeneans. International Journal for Parasitology 27, 1289–1297.CrossRefGoogle ScholarPubMed
Littlewood, DT, Curini-Galletti, M and Herniou, EA (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution 16, 449–466.CrossRefGoogle ScholarPubMed
Locke, SA, McLaughlin, JD and Marcogliese, DJ (2010a) DNA barcodes show cryptic diversity and a potential physiological basis for host specificity among Diplostomoidea (Platyhelminthes: Digenea) parasitizing freshwater fishes in the St. Lawrence River, Canada. Molecular Ecology 19, 2813–2827.CrossRefGoogle Scholar
Locke, SA, McLaughlin, JD, Dayanandan, S and Marcogliese, DJ (2010b) Diversity, specificity and evidence of hybridization in Diplostomum spp. metacercariae in freshwater fishes is revealed by DNA barcodes and ITS sequences. International Journal for Parasitology 40, 333–343.CrossRefGoogle Scholar
Locke, SA, Al-Nasiri, FS, Caffara, M, Drago, F, Kalbe, M, Lapierre, AR, McLaughlin, JD, Nie, P, Overstreet, RM, Souza, GTR, Takemoto, RM and Marcogliese, DJ (2015) Diversity, specificity and speciation in larval Diplostomidae (Platyhelminthes: Digenea) in the eyes of freshwater fish, as revealed by DNA barcodes. International Journal for Parasitology 45, 841–855.CrossRefGoogle ScholarPubMed
Locke, SA, Drago, FB, Núñez, V, Souza, GTRE and Takemoto, RM (2020) Phylogenetic position of Diplostomum spp. from New World herons based on complete mitogenomes, rDNA operons, and DNA barcodes, including a new species with partially elucidated life cycle. Parasitology Research 119, 2129–2137.CrossRefGoogle ScholarPubMed
McKeown, CA and Irwin, SWB (1995) The life cycle stages of three Diplostomum species maintained in the laboratory. International Journal for Parasitology 25, 897–906.CrossRefGoogle ScholarPubMed
Moszczynska, A, Locke, SA, McLaughlin, JD, Marcogliese, DJ and Crease, TJ (2009) Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Molecular Ecology Resources 9, 75–82.CrossRefGoogle ScholarPubMed
Niewiadomska, K (2002) Family Diplostomidae Poirier 1886. In Gibson, DI, Jones, A and Bray, RA (eds), Keys to the Trematoda. London, Wallingford: CABI, Natural History Museum, pp. 167–196.CrossRefGoogle Scholar
Niewiadomska, K (2010) Fauna słodkowodna Polski. 34A. Przywry (Trematoda). Część ogólna; Część systematyczna – Aspidogastrea, Digenea: Strigeida. Łódź: Wydawnictwo Uniwersytetu Łódzkiego (in Polish).CrossRefGoogle Scholar
Niewiadomska, K and Kiseliene, V (1990) Diplostomum baeri Dubois, 1937 (Digenea, Diplostomidae) from Lithuania. Acta Parasitologica Polonica 35, 277–283.Google Scholar
Niewiadomska, K and Kiseliene, V (1994) Diplostomum cercariae (Digenea) in snails from Lithuania. II. Survey of species. Acta Parasitologica 39, 179–186.Google Scholar
Niewiadomska, K and Laskowski, Z (2002) Systematic relationships among six species of Diplostomum Nordmann, 1832 (Digenea) based on morphological and molecular data. Acta Parasitologica 47, 20–28.Google Scholar
Olson, PD and Tkach, VV (2005) Advances and trends in the molecular systematics of the parasitic Platyhelminthes. Advances in Parasitology 60, 165–243.CrossRefGoogle ScholarPubMed
Pantoja, C, Faltýnková, A, O'Dwyer, K, Jouet, D, Skírnisson, K and Kudlai, O (2021) Diversity of echinostomes (Digenea: Echinostomatidae) in their snail hosts in high latitudes. Parasite 28, 59.CrossRefGoogle ScholarPubMed
Pérez-del-Olmo, A, Georgieva, S, Pula, HJ and Kostadinova, A (2014) Molecular and morphological evidence for three species of Diplostomum (Digenea: Diplostomidae), parasites of fishes and fish-eating birds in Spain. Parasites & Vectors 7, 502.CrossRefGoogle Scholar
Pleijel, F, Jondelius, U, Norlinder, E, Nygren, A, Oxelman, B, Schander, C, Sundberg, P and Thollesson, M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution 48, 369–371.CrossRefGoogle Scholar
Rambaut, A (2012) FigTree v1. 4. Molecular evolution, phylogenetics and epidemiology. Available at http://tree.bio.ed.ac.uk/software/figtree/ (Accessed 1 February 2021).Google Scholar
Rellstab, C, Louhi, K-R, Karvonen, A and Jokela, J (2011) Analysis of trematode parasite communities in fish eye lenses by pyrosequencing of naturally pooled DNA. Infection, Genetics and Evolution 11, 1276–1286.CrossRefGoogle ScholarPubMed
Ronquist, F, Teslenko, M, Van Der Mark, P, Ayres, DL, Darling, A, Höhna, S and Huelsenbeck, JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Rozas, J, Sánchez-DelBarrio, JC, Messeguer, X and Rozas, R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics (Oxford, England) 12, 2496–2497.CrossRefGoogle Scholar
Schwelm, J, Georgieva, S, Grabner, D, Kostadinova, A and Sures, B (2021) Molecular and morphological characterisation of Diplostomum phoxini (Faust, 1918) with a revised classification and an updated nomenclature of the species-level lineages of Diplostomum (Digenea: Diplostomidae) sequenced worldwide. Parasitology 148, 1648–1664. doi: 10.1017/S0031182021001372CrossRefGoogle Scholar
Selbach, C, Soldánová, M, Georgieva, S, Kostadinova, A and Sures, B (2015) Integrative taxonomic approach to the cryptic diversity of Diplostomum spp. in lymnaeid snails from Europe with a focus on the ‘Diplostomum mergi’ species complex. Parasites & Vectors 8, 300.CrossRefGoogle Scholar
Shaffer, MR, Davy, SK and Bell, JJ (2019) Hidden diversity in the genus Tethya: comparing molecular and morphological techniques for species identification. Heredity 122, 354–369.CrossRefGoogle ScholarPubMed
Shigin, AA (1968) On the study of life cycle and morphology of the cercaria Diplostomum indistinctum (Trematoda, Diplostomatidae). Trudy GELAN SSSR 19, 208–217 (in Russian).Google Scholar
Shigin, AA (1977) Morphology, biology and taxonomy of Diplostomum from Palearctic Laridae. Trudy GELAN SSSR 27, 5–64 (in Russian).Google Scholar
Shigin, AA (1986) Trematodes in the fauna of the USSSR: the genus Diplostomum. Metacercariae. Moscow: Nauka (in Russian).Google Scholar
Shigin, AA (1993) Trematodes of the fauna of Russia and neighbouring regions. Genus Diplostomum. Adults. Moscow: Nauka (in Russian).Google Scholar
Snyder, SD and Tkach, VV (2001) Phylogenetic and biogeographical relationships among some Holarctic frog lung flukes (Digenea: Haematoloechidae). The Journal of Parasitology 87, 1433–1440.CrossRefGoogle Scholar
Tautz, D, Arctander, P, Minelli, A, Thomas, RH and Vogler, AP (2003) A plea for DNA taxonomy. Trends in Ecology & Evolution 18, 70–74.CrossRefGoogle Scholar
Thompson, CW, Phelps, KL, Allard, MW, Cook, JA, Dunnum, JL, Ferguson, AW, Gelang, M, Khan, FAA, Paul, DL, Reeder, DM, Simmons, NB, Vanhove, MPM, Webala, PW, Weksler, M and Kilpatrick, CW (2021) Preserve a voucher specimen! The critical need for integrating natural history collections in infectious disease studies. Host-Microbe Biology 12, e02698–20.Google ScholarPubMed
Tkach, VV, Littlewood, DT, Olson, PD, Kinsella, JM and Swiderski, Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56, 1–15.CrossRefGoogle Scholar
Unger, P and Palm, HW (2017) Parasite risk of maricultured rainbow trout (Oncorhynchus mykiss Walbaum, 1792) in the Western Baltic Sea, Germany. Aquaculture International 25, 975–989.CrossRefGoogle Scholar
Valkiūnas, G, Atkinson, CT, Bensch, S, Sehgal, RN and Ricklefs, RE (2008) Parasite misidentifications in GenBank: how to minimize their number? Trends in Parasitology 24, 247–248.CrossRefGoogle ScholarPubMed
van Steenkiste, N, Locke, SA, Castelin, M, Marcogliese, DJ and Abbott, CL (2015) New primers for DNA barcoding of digeneans and cestodes (Platyhelminthes). Molecular Ecology Resources 15, 945–952.CrossRefGoogle Scholar
Vilgalys, R (2003) Taxonomic misidentification in public DNA databases. New Phytologist 160, 4–5.CrossRefGoogle ScholarPubMed
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