Hostname: page-component-745bb68f8f-5r2nc Total loading time: 0 Render date: 2025-01-13T19:34:12.841Z Has data issue: false hasContentIssue false

Complex species structure of Lecithaster salmonis (Digenea: Lecithasteridae), a fish parasite in the Arctic and Pacific Northwest

Published online by Cambridge University Press:  13 January 2025

D. Krupenko*
Affiliation:
Laboratory of Parasitic Worms and Protists, Zoological Institute of the Russian Academy of Sciences, Universitetskaya nab. 1, 199034, Saint Petersburg, Russia Department of Invertebrate Zoology, Saint Petersburg University, Universitetskaya nab. 7–9, 199034, Saint Petersburg, Russia
A. Gonchar
Affiliation:
Laboratory of Parasitic Worms and Protists, Zoological Institute of the Russian Academy of Sciences, Universitetskaya nab. 1, 199034, Saint Petersburg, Russia Department of Invertebrate Zoology, Saint Petersburg University, Universitetskaya nab. 7–9, 199034, Saint Petersburg, Russia
V. Krapivin
Affiliation:
Department of Invertebrate Zoology, Saint Petersburg University, Universitetskaya nab. 7–9, 199034, Saint Petersburg, Russia Center of Parasitology of A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, Leninskii Prospect 33, 117071, Moscow, Russia
G. Kremnev
Affiliation:
Laboratory of Parasitic Worms and Protists, Zoological Institute of the Russian Academy of Sciences, Universitetskaya nab. 1, 199034, Saint Petersburg, Russia
O. Skobkina
Affiliation:
Laboratory of Parasitic Worms and Protists, Zoological Institute of the Russian Academy of Sciences, Universitetskaya nab. 1, 199034, Saint Petersburg, Russia
B. Efeykin
Affiliation:
Center of Parasitology of A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, Leninskii Prospect 33, 117071, Moscow, Russia
*
Corresponding author: D. Krupenko; Email: krupenko.d@gmail.com

Abstract

Studying complexes of cryptic or pseudocryptic species opens new horizons for the understanding of speciation processes, an important yet vague issue for the digeneans. We investigated a hemiuroidean trematode Lecithaster salmonis across a wide geographic range including the northern European seas (White, Barents, and Pechora), East Siberian Sea, and the Pacific Northwest (Sea of Okhotsk and Sea of Japan). The goals were to explore the genetic diversity within L. salmonis through mitochondrial (cox1 and nad5 genes) and ribosomal (ITS1, ITS2, 28S rDNA) marker sequences, to study morphometry of maritae, and to revise the life cycle data. Mitochondrial markers showed that L. salmonis is likely divided into six lineages (referred to as operational taxonomic units, OTUs), which often occur in sympatry, sometimes in a single host specimen. Variation in rDNA was not consistent with that in the mitochondrial markers. Morphometric analysis of maritae was performed for four out of six OTUs; it showed that some OTUs had significant differences from the others, but some did not. The effect of host species on the morphometric characteristics cannot be excluded. Intramolluscan stages were identified for two OTUs; they differed clearly by the structure of cercariae and also by the species of the first intermediate host. The case of L. salmonis is instructive in how different criteria for species delimitation can contradict each other. We regard this as a sign of recent or ongoing speciation and suggest using the name Lecithaster cf. salmonis. The most promising criteria to differentiate genetic lineages within L. cf. salmonis are first intermediate hosts and morphological characteristics of the cercariae: shape of the delivery tube and caudal cyst, and length of the filamentous appendage.

Type
Research Paper
Copyright
© The Author(s), 2025. 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

Atopkin, DM, Nakao, M, Besprozvannykh, VV, Ha, ND, Nguyen, HV and Sasaki, M (2020) 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. Journal of Helminthology 94, e14. https://doi.org/10.1017/S0022149X18001049.CrossRefGoogle Scholar
Bayssade-Dufour, C, Jouet, D, Rudolfova, J, Horák, P and Ferté, H (2006) Seasonal morphological variations in bird schistosomes. Parasite 13(3), 205214. https://doi.org/10.1051/parasite/2006133205.CrossRefGoogle ScholarPubMed
Bik, HM, Fournier, D, Sung, W, Bergeron, RD and Thomas, WK (2013) Intra-genomic variation in the ribosomal repeats of nematodes. PLoS One 8(10), e78230. https://doi.org/10.1371/journal.pone.0078230.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. Advances in Parasitology 98, 167225. https://doi.org/10.1016/bs.apar.2017.05.001.CrossRefGoogle ScholarPubMed
Blasco-Costa, I and Poulin, R (2017) Parasite life-cycle studies: A plea to resurrect an old parasitological tradition. Journal of Helminthology 91(6), 647656. https://doi.org/10.1017/S0022149X16000924.CrossRefGoogle ScholarPubMed
Bouckaert, R, Vaughan, TG, Barido-Sottani, J, Duchêne, S, Fourment, M, Gavryushkina, A, Heled, J, Jones, G, Kühnert, D, De Maio, N, Matschiner, M, Mendes, FK, Müller, NF, Ogilvie, HA, Du Plessis, L, Popinga, A, Rambaut, A, Rasmussen, D, Siveroni, I, Suchard, MA, Wu, C-H, Xie, D, Zhang, C, Stadler, T and Drummond, AJ (2019) BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLOS Computational Biology 15(4), e1006650. https://doi.org/10.1371/journal.pcbi.1006650.CrossRefGoogle ScholarPubMed
Bouckaert, RR and Drummond, AJ (2017) bModelTest: Bayesian phylogenetic site model averaging and model comparison. BMC Evolutionary Biology 17(1), 42. https://doi.org/10.1186/s12862-017-0890-6.CrossRefGoogle ScholarPubMed
Bouguerche, C, Huston, DC, Karlsbakk, E, Ahmed, M and Holovachov, O (2024) Untangling the Derogenes varicus species complex in Scandinavian waters and the Arctic: Description of Derogenes abba n. sp. (Trematoda, Derogenidae) from Hippoglossoides platessoides and new host records for D. varicus (Müller, 1784) sensu stricto. Parasite 31, 26. https://doi.org/10.1051/parasite/2024024.CrossRefGoogle Scholar
Boyce, NPJ (1969) Parasite fauna of pink salmon (Oncorhynchus gorbuscha) of the Bella Coola River, Central British Columbia, during their early sea life. Journal of the Fisheries Research Board of Canada 26(4), 813820. https://doi.org/10.1139/f69-079.CrossRefGoogle Scholar
Bray, RA, Cutmore, SC and Cribb, TH (2022) A paradigm for the recognition of cryptic trematode species in tropical Indo-west Pacific fishes: The problematic genus Preptetos (Trematoda: Lepocreadiidae). International Journal for Parasitology 52(2–3), 169203. https://doi.org/10.1016/j.ijpara.2021.08.004.CrossRefGoogle ScholarPubMed
Briscoe, AG, Bray, RA, Brabec, J and Littlewood, DTJ (2016) The mitochondrial genome and ribosomal operon of Brachycladium goliath (Digenea: Brachycladiidae) recovered from a stranded minke whale. Parasitology International 65(3), 271275. https://doi.org/10.1016/j.parint.2016.02.004.CrossRefGoogle ScholarPubMed
Carranza, S, Baguñà, J and Riutort, M (1999) Origin and evolution of paralogous rRNA gene clusters within the flatworm family Dugesiidae (Platyhelminthes, Tricladida). Journal of Molecular Evolution 49(2), 250259. https://doi.org/10.1007/PL00006547.CrossRefGoogle ScholarPubMed
Charkin, AN, Kosobokova, KN, Ershova, EA, Syomin, VL, Kolbasova, GD, PYu, Semkin, Leusov, AE, Dudarev, OV, Gulenko, TA, Yaroshchuk, EI, Startsev, AM, Fayman, PA, Krasikov, VA, Zverev, SA, Bessonova, EA, Ulyantsev, AS, Elovsky, EV, Yurikova, DA, Kobyakov, KA, Zimina, OL, Gerasimova, AV, Tishchenko, PP and Didov, AA (2024) A unique warm–water oasis in the Siberian Arctic’s Chaun Bay sustained by hydrothermal groundwater discharge. Communications Earth & Environment 5(1), 393. https://doi.org/10.1038/s43247-024-01529-x.CrossRefGoogle Scholar
Chernov, I and Tolstikov, A (2020) The White Sea: Available data and numerical models. Geosciences 10(11), 463. https://doi.org/10.3390/geosciences10110463.CrossRefGoogle Scholar
Ching, HL (1960) Studies on three Hemiuroid Cercariae from Friday Harbor, Washington. Journal of Parasitology 46(5), 663. https://doi.org/10.2307/3274959.CrossRefGoogle ScholarPubMed
Clement, M, Snell, Q, Walke, P, Posada, D and Crandall, K (2002) TCS: Estimating gene genealogies. In Proceedings 16th International Parallel and Distributed Processing Symposium. Ft. Lauderdale, FL: IEEE, 7 pp. https://doi.org/10.1109/IPDPS.2002.1016585.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. https://doi.org/10.1016/S0020-7519(98)00127-1.CrossRefGoogle ScholarPubMed
Cribb, TH, Bray, RA, Justine, J-L, Reimer, J, Sasal, P, Shirakashi, S and Cutmore, SC (2022) A world of taxonomic pain: Cryptic species, inexplicable host-specificity, and host-induced morphological variation among species of Bivesicula Yamaguti, 1934 (Trematoda: Bivesiculidae) from Indo-Pacific Holocentridae, Muraenidae and Serranidae. Parasitology 149(6), 831853. https://doi.org/10.1017/S0031182022000282.CrossRefGoogle ScholarPubMed
Cribb, TH, Cutmore, SC and Bray, RA (2021) The biodiversity of marine trematodes: Then, now and in the future. International Journal for Parasitology 51(13–14), 10851097. https://doi.org/10.1016/j.ijpara.2021.09.002.CrossRefGoogle ScholarPubMed
Cutmore, SC, Corner, RD and Cribb, TH (2023) Morphological constraint obscures richness: A mitochondrial exploration of cryptic richness in Transversotrema (Trematoda: Transversotrematidae). International Journal for Parasitology 53(11–12), 595635. https://doi.org/10.1016/j.ijpara.2023.06.006.CrossRefGoogle ScholarPubMed
Galaktionov, KV, Blasco-Costa, I and Olson, PD (2012) Life cycles, molecular phylogeny and historical biogeography of the ‘pygmaeus’ microphallids (Digenea: Microphallidae): Widespread parasites of marine and coastal birds in the Holarctic. Parasitology 139(10), 13461360. https://doi.org/10.1017/S0031182012000583.CrossRefGoogle ScholarPubMed
Hildebrand, J, Adamczyk, M, Laskowski, Z and Zaleśny, G (2015) Host-dependent morphology of Isthmiophora melis (Schrank, 1788) Luhe, 1909 (Digenea, Echinostomatinae) – morphological variation vs. molecular stability. Parasites & Vectors 8(1), 481. https://doi.org/10.1186/s13071-015-1095-8.CrossRefGoogle ScholarPubMed
Hoang, DT, Chernomor, O, von Haeseler, A, Minh, BQ and Vinh, LS (2018) UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35(2), 518522. https://doi.org/10.1093/molbev/msx281.CrossRefGoogle ScholarPubMed
Høisæter, T (2014) The Pyramidellidae (Gastropoda, Heterobranchia) of Norway and adjacent waters. A taxonomic review. Fauna Norvegica 34, 778. https://doi.org/10.5324/fn.v34i0.1672.CrossRefGoogle Scholar
Hunninen, AV and Cable, RM (1943) The life history of Lecithaster confusus Odhner (Trematoda: Hemiuridae). Journal of Parasitology 29(1), 71. https://doi.org/10.2307/3272751.CrossRefGoogle Scholar
Issaitschikov, IM (1933) Contributions to the knowledge of parasitic helminths of some groups of vertebrates in the Russian Arctic. A. Trematodes (part 2). Trudy Gosudarstvennogo Okeanograficheskogo Instituta 3(1), 344 (in Russian with English summary).Google Scholar
Kantor, YI and Sysoev, AV (2006) Marine and Brackish Water Gastropoda of Russia and Adjacent Countries: An Illustrated Catalogue. Moscow: KMK Scientific Press Ltd.Google Scholar
Keller, I, Chintauan-Marquier, IC, Veltsos, P and Nichols, RA (2006) Ribosomal DNA in the Grasshopper Podisma pedestris: Escape from concerted evolution. Genetics 174(2), 863874. https://doi.org/10.1534/genetics.106.061341.CrossRefGoogle ScholarPubMed
Køie, M (1989) On the morphology and life history of Lecithaster gibbosus (Rudolphi, 1802) Lühe, 1901 (Digenea, Hemiuroidea). Parasitology Research 75(5), 361367. https://doi.org/10.1007/BF00931131.CrossRefGoogle Scholar
Krupenko, D, Kremnev, G, Gonchar, A, Uryadova, A, Miroliubov, A, Krapivin, V, Skobkina, O, Gubler, A and Knyazeva, O (2022a) Species complexes and life cycles of digenetic trematodes from the family Derogenidae. Parasitology 149(12), 15901606. https://doi.org/10.1017/S003118202200110X.CrossRefGoogle ScholarPubMed
Krupenko, D, Kremnev, G, Skobkina, O, Gonchar, A, Uryadova, A and Miroliubov, A (2022b) Lecithaster (Lecithasteridae, Digenea) in the White Sea: An unnoticed guest from the Pacific? Journal of Helminthology 96, e43. https://doi.org/10.1017/S0022149X22000281.CrossRefGoogle Scholar
Laakkonen, HM, Hardman, M, Strelkov, P and Väinölä, R (2021) Cycles of trans‐Arctic dispersal and vicariance, and diversification of the amphi‐boreal marine fauna. Journal of Evolutionary Biology 34(1), 7396. https://doi.org/10.1111/jeb.13674.CrossRefGoogle ScholarPubMed
Leigh, JW and Bryant, D (2015) PopART: Full‐feature software for haplotype network construction. Methods in Ecology and Evolution 6(9), 11101116. https://doi.org/10.1111/2041-210X.12410.CrossRefGoogle 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(2), 323327. https://doi.org/10.1016/0166-6851(92)90181-I.CrossRefGoogle ScholarPubMed
Nguyen, L-T, Schmidt, HA, von Haeseler, A and Minh, BQ (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32(1), 268274. https://doi.org/10.1093/molbev/msu300.CrossRefGoogle ScholarPubMed
Morgan, JAT and Blair, D (1995) Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: An aid to establishing relationships within the 37-collar-spine group. Parasitology 111(5), 609615. https://doi.org/10.1017/S003118200007709X.CrossRefGoogle ScholarPubMed
Odhner, T (1905) Die Trematoden des arktischen Gebietes. Leipzig: G. Fischer. https://doi.org/10.5962/bhl.title.11724 (in German).Google Scholar
Olson, PD, Cribb, TH, Tkach, Bray RA VV and Littlewood, DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33(7), 733755. https://doi.org/10.1016/S0020-7519(03)00049-3.CrossRefGoogle ScholarPubMed
Oksanen, J, Simpson, G, Blanchet, F, Kindt, R, Legendre, P, Minchin, P, O’Hara, R, Solymos, P, Stevens, M, Szoecs, E, Wagner, H, Barbour, M, Bedward, M, Bolker, B, Borcard, D, Carvalho, G, Chirico, M, De Caceres, M, Durand, S, Evangelista, H, FitzJohn, R, Friendly, M, Furneaux, B, Hannigan, G, Hill, M, Lahti, L, McGlinn, D, Ouellette, M, Ribeiro Cunha, E, Smith, T, Stier, A, Ter Braak, C and Weedon, J (2022). vegan: Community Ecology Package. R package version 2.6-4, https://CRAN.R-project.org/package=vegan.Google Scholar
Pérez-Ponce De León, G and Poulin, R (2018) An updated look at the uneven distribution of cryptic diversity among parasitic helminths. Journal of Helminthology 92(2), 197202. https://doi.org/10.1017/S0022149X17000189.CrossRefGoogle Scholar
Pérez-Ponce De León, G, Solórzano-García, B, Huston, DC, Mendoza-Garfias, B, Cabañas-Granillo, J, Cutmore, SC and Cribb, TH (2024) Molecular species delimitation of marine trematodes over wide geographical ranges: Schikhobalotrema spp. (Digenea: Haplosplanchnidae) in needlefishes (Belonidae) from the Pacific Ocean and Gulf of Mexico. Parasitology 151(2):168180. https://doi.org/10.1017/S0031182023001245.Google ScholarPubMed
Puillandre, N, Brouillet, S and Achaz, G (2021) ASAP: Assemble species by automatic partitioning. Molecular Ecology Resources 21(2), 609620. https://doi.org/10.1111/1755-0998.13281.CrossRefGoogle ScholarPubMed
Quinn, GP and Keough, MJ (2002) Experimental Design and Data Analysis for Biologists. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Team, R Core (2023) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. https://www.R-project.org/.Google Scholar
Rambaut, A, Drummond, AJ, Xie, D, Baele, G and Suchard, MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67(5), 901904. https://doi.org/10.1093/sysbio/syy032.CrossRefGoogle ScholarPubMed
Schindelin, J, Arganda-Carreras, I, Frise, E, Kaynig, V, Longair, M, Pietzsch, T, Preibisch, S, Rueden, C, Saalfeld, S, Schmid, B, Tinevez, J-Y, White, DJ, Hartenstein, V, Eliceiri, K, Tomancak, P and Cardona, A (2012) Fiji: An open-source platform for biological-image analysis. Nature Methods 9(7), 676682. https://doi.org/10.1038/nmeth.2019.CrossRefGoogle ScholarPubMed
Shulman, S and Shulman-Albova, R (1953) Parasites of Fishes of the White Sea. Moskva-Leningrad, Izdatelstvo Akademia Nauk SSSR (in Russian).Google Scholar
Simon, UK and Weiss, M (2008) Intragenomic variation of fungal ribosomal genes is higher than previously thought. Molecular Biology and Evolution 25(11), 22512254. https://doi.org/10.1093/molbev/msn188.CrossRefGoogle Scholar
Stunkard, HW (1957) Intraspecific variation in parasitic flatworms. Systematic Zoology 6(1), 7. https://doi.org/10.2307/2411703.CrossRefGoogle Scholar
Sukhotin, A, Denisenko, S and Galaktionov, K (2019) Pechora Sea ecosystems: Current state and future challenges. Polar Biology 42(9), 16311645. https://doi.org/10.1007/s00300-019-02553-w.CrossRefGoogle Scholar
Tamura, K, Stecher, G and Kumar, S (2021) MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution 38(7), 30223027. https://doi.org/10.1093/molbev/msab120.CrossRefGoogle ScholarPubMed
Tang, Y, Horikoshi, M and Li, W (2016) ggfortify: Unified interface to visualize statistical results of popular R packages. The R Journal 8(2), 474. https://doi.org/10.32614/RJ-2016-060.CrossRefGoogle Scholar
Tkach, V, Grabda-Kazubska, B, Pawlowski, J and Swiderski, Z (1999) Molecular and morphological evidence for close phylogenetic affinities of the genera Macrodera, Leptophallus, Metaleptophallus and Paralepoderma (Digenea, Plagiorchiata). Acta Parasitologica 44, 170179.Google Scholar
Wickham, H (2016) ggplot2: Elegant Graphics for Data Analysis. New York: Springer-Verlag.CrossRefGoogle Scholar
Yamaguti, S (1934) Studies on the helminth fauna of Japan. Part 2, Trematodes of fishes, I. Japanese Journal of Zoology 5, 249541.Google Scholar
Zhukov, EV (1960) Endoparasitic worms of fish from the Sea of Japan and the shallow waters of the South Kuril Islands. Trudy Zoologicheskogo Instituta ANSSR 28, 3146 (in Russian with English summary).Google Scholar
Zhukov, EV (1963) Parasite fauna of fish in Chukotka. Part II. Endoparasites of marine and fresh-water fish. Parazitologicheski Sbornik 21, 96139 (in Russian with English summary).Google Scholar
Supplementary material: File

Krupenko et al. supplementary material 1

Krupenko et al. supplementary material
Download Krupenko et al. supplementary material 1(File)
File 17.1 KB
Supplementary material: File

Krupenko et al. supplementary material 2

Krupenko et al. supplementary material
Download Krupenko et al. supplementary material 2(File)
File 16.1 KB