Diversity and phylogenetic relationships of European species of  Crepidostomum  Braun, 1900 (Trematoda: Allocreadiidae) based on rDNA, with special reference to  Crepidostomum oschmarini  Zhokhov & Pugacheva, 1998

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Abstract

Background

Within the genus Crepidostomum Braun, 1900, identification of species and taxonomic decisions made only on the basis of adult morphology have resulted in great problems associated with evaluating actual diversity and validity of species. Life-cycle data, while equal in importance to adult characters, are scarce, controversial or incomplete for most Crepidostomum spp. In this study, rDNA sequences generated from adult and larval Crepidostomum spp. and some other allocreadiid species were analysed to reveal the diversity and phylogenetic relationships of the species and their host range. Detailed morphological description based on light microscopy, SEM tegumental surface topography and genetic data are provided for the poorly known trematode C. oschmarini Zhokhov & Pugacheva, 1998 found in the intestine of two teleost fish species, Barbatula barbatula (L.) and Cottus gobio L.

Results

We characterized 27 isolates of adult and larval parasites. Based on newly obtained 28S and ITS1- 5.8S-ITS2 rDNA sequences, new intermediate and final hosts were ascertained, and life-cycles clarified for some allocreadiids. New knowledge on the diversity and phylogenetic relationships of European Crepidostomum spp. was gained. The validity of C. oschmarini was verified based on comparative sequence analysis. Ophthalmoxiphidiocercariae of C. oschmarini were recorded in sphaeriid bivalves Pisidium ( Euglesa) casertanum (Poli) . Additionally, morphological differences between gravid specimens of C. oschmarini and other related species were observed.

Conclusions

Species of the Allocreadiidae parasitizing fishes in Europe are distributed among two monophyletic genera, Allocreadium and Bunodera, and two paraphyletic Crepidostomum clades. A complex of Crepidostomum metoecus (syn. C. nemachilus), C. oschmarini and Crepidostomum sp. 2 clustered in one clade, and a complex of C. farionis, Crepidostomum sp. 1 and, probably, C. wikgreni in the other. Molecular data indicated that C. oschmarini and Crepidostomum sp. 2 presumably have a wide geographical distribution in Europe. The new data provided evidence that Crepidostomum is a more diverse genus than can be judged from morphological data and host switching in this genus may occur independently of fish-host phylogeny.

Related collections

Most cited references 45

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Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda).

D. Timothy J. Littlewood, Thomas Olson, R Bray … (2003)

Complete small subunit ribosomal RNA gene (ssrDNA) and partial (D1-D3) large subunit ribosomal RNA gene (lsrDNA) sequences were used to estimate the phylogeny of the Digenea via maximum parsimony and Bayesian inference. Here we contribute 80 new ssrDNA and 124 new lsrDNA sequences. Fully complementary data sets of the two genes were assembled from newly generated and previously published sequences and comprised 163 digenean taxa representing 77 nominal families and seven aspidogastrean outgroup taxa representing three families. Analyses were conducted on the genes independently as well as combined and separate analyses including only the higher plagiorchiidan taxa were performed using a reduced-taxon alignment including additional characters that could not be otherwise unambiguously aligned. The combined data analyses yielded the most strongly supported results and differences between the two methods of analysis were primarily in their degree of resolution. The Bayesian analysis including all taxa and characters, and incorporating a model of nucleotide substitution (general-time-reversible with among-site rate heterogeneity), was considered the best estimate of the phylogeny and was used to evaluate their classification and evolution. In broad terms, the Digenea forms a dichotomy that is split between a lineage leading to the Brachylaimoidea, Diplostomoidea and Schistosomatoidea (collectively the Diplostomida nomen novum (nom. nov.)) and the remainder of the Digenea (the Plagiorchiida), in which the Bivesiculata nom. nov. and Transversotremata nom. nov. form the two most basal lineages, followed by the Hemiurata. The remainder of the Plagiorchiida forms a large number of independent lineages leading to the crown clade Xiphidiata nom. nov. that comprises the Allocreadioidea, Gorgoderoidea, Microphalloidea and Plagiorchioidea, which are united by the presence of a penetrating stylet in their cercariae. Although a majority of families and to a lesser degree, superfamilies are supported as currently defined, the traditional divisions of the Echinostomida, Plagiorchiida and Strigeida were found to comprise non-natural assemblages. Therefore, the membership of established higher taxa are emended, new taxa erected and a revised, phylogenetically based classification proposed and discussed in light of ontogeny, morphology and taxonomic history.

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Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea).

Vasyl Tkach, D. Timothy J. Littlewood, Peter D. Olson … (2003)

Phylogenetic interrelationships of 32 species belonging to 18 genera and four families of the superfamily Microphalloidea were studied using partial sequences of nuclear lsrDNA analysed by Bayesian inference and maximum parsimony. The resulting trees were well resolved at most nodes and demonstrated that the Microphalloidea, as represented by the present data-set, consists of three main clades corresponding to the families Lecithodendriidae, Microphallidae and Pleurogenidae + Prosthogonimidae. Interrelationships of taxa within each clade are considered; as a result of analysis of molecular and morphological data, Floridatrema Kinsella & Deblock, 1994 is synonymised with Maritrema Nicoll, 1907, Candidotrema Dollfus, 1951 with Pleurogenes Looss, 1896, and Schistogonimus Lühe, 1909 with Prosthogonimus Lühe, 1899. The taxonomic value of some morphological features, used traditionally for the differentiation of genera within the Lecithodendriidae and Prosthogonimidae, is reconsidered. Previous systematic schemes are discussed from the viewpoint of present results, and perspectives of future studies are outlined.

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A molecular phylogeny of the human schistosomes.

David McManus, Carol D. Blair, Erin J. Aiello Bowles (1995)

Members of the genus Schistosoma are generally grouped on the basis of egg morphology, intermediate host specificity, and geographic origin. We have tested hypotheses based on these groupings by phylogenetic analysis of nuclear ribosomal (ITS2) and mitochondrial (COI) nucleotide sequences. Both mitochondrial and nuclear DNA data strongly support "traditional" hypotheses that (a) members of the Schistosoma haematobium group form a monophyletic clade, (b) members of the S. mansoni group form a monophyletic clade, (c) S. japonicum and S. mekongi form a monophyletic group relative to other schistosomes, and (d) the African schistosomes form a clade to the exclusion of the two Asian species.

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Author and article information

Contributors

Romualda Petkevičiūtė: romualda.petkeviciute@gamtc.lt

Virmantas Stunžėnas: virmantas.stunzenas@gamtc.lt

Alexander E. Zhokhov: aezhokhov@yandex.ru

Larisa G. Poddubnaya: poddubny@ibiw.yaroslavl.ru

Gražina Stanevičiūtė: grazina.staneviciute@gamtc.lt

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 28 September 2018

Publication date PMC-release: 28 September 2018

Publication date Collection: 2018

Volume: 11

Electronic Location Identifier: 530

Affiliations

[1 ]ISNI 0000 0004 0522 3211, GRID grid.435238.b, Institute of Ecology of Nature Research Centre, ; Akademijos str. 2, LT-08412 Vilnius, Lithuania

[2 ]ISNI 0000 0001 2192 9124, GRID grid.4886.2, Papanin Institute for Biology of Inland Waters, , Russian Academy of Sciences, ; Borok, Russia

Article

Publisher ID: 3095

DOI: 10.1186/s13071-018-3095-y

PMC ID: 6162956

PubMed ID: 30266086

SO-VID: ba71aa9e-bec3-4545-842f-c3ffb04cbc38

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 13 April 2018

Date accepted : 3 September 2018

Funding

Funded by: Lietuvos Mokslo Taryba (LT)

Award ID: MIP-43/2015

Award Recipient : Virmantas Stunžėnas

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: crepidostomum oschmarini,its2 rdna,28s,molecular phylogeny,life-cycles,tegumental topography,morphology,stone loach barbatula barbatula,european bullhead cottus gobio

Data availability:

ScienceOpen disciplines: Parasitology

Keywords: crepidostomum oschmarini, its2 rdna, 28s, molecular phylogeny, life-cycles, tegumental topography, morphology, stone loach barbatula barbatula, european bullhead cottus gobio

Diversity and phylogenetic relationships of European species of Crepidostomum Braun, 1900 (Trematoda: Allocreadiidae) based on rDNA, with special reference to Crepidostomum oschmarini Zhokhov & Pugacheva, 1998

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Ticks and tick-borne pathogens

Most cited references 45

Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda).

Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea).

A molecular phylogeny of the human schistosomes.

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