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The tapeworm Atractolytocestus tenuicollis (Cestoda: Caryophyllidea)—a sister species or ancestor of an invasive A. huronensis?

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Abstract

Atractolytocestus tenuicollis (Li, 1964) Xi, Wang, Wu, Gao et Nie, 2009 is a monozoic, non-segmented tapeworm of the order Caryophyllidea, parasitizing exclusively common carp (Cyprinus carpio L.). In the current work, the first molecular data, in particular complete ribosomal internal transcribed spacer 2 (ITS2) and partial mitochondrial cytochrome c oxidase subunit I (cox1) on A. tenuicollis from Niushan Lake, Wuhan, China, are provided. In order to evaluate molecular interrelationships within Atractolytocestus, the data on A. tenuicollis were compared with relevant data on two other congeners, Atractolytocestus huronensis and Atractolytocestus sagittatus. Divergent intragenomic copies (ITS2 paralogues) were detected in the ITS2 ribosomal spacer of A. tenuicollis; the same phenomenon has previously been observed also in two other congeners. ITS2 structure of A. tenuicollis was very similar to that of A. huronensis from Slovakia, USA and UK; overall pairwise sequence identity was 91.7–95.2 %. On the other hand, values of sequence identity between A. tenuicollis and A. sagittatus were lower, 69.7–70.9 %. Cox1 sequence, analysed in five A. tenuicollis individuals, were 100 % identical and no intraspecific variation was observed. Comparison of A. tenuicollis cox1 with respective sequences of two other Atractolytocestus species showed that the mitochondrial haplotype found in Chinese A. tenuicollis is structurally specific (haplotype 4; Ha4) and differs from all so far determined Atractolytocestus haplotypes (Ha1 and Ha2 for A. huronensis; Ha3 for A. sagittatus). Pairwise sequence identity between A. tenuicollis cox1 haplotype and remaining three haplotypes followed the same pattern as in ITS2. The nucleotide and amino acide (aa) sequence comparison with A. huronensis Ha1 and Ha2 revealed higher sequence identity, 90.3–90.8 % (96.9 % in aa), while lower values were achieved between A. tenuicollis haplotype and Ha3 of Japanese A. sagittatus—75.2 % (81.9 % in aa). The phylogenetic analyses using cox1, ITS2 and combined cox1 + ITS2 sequences revealed close genetic interrelationship between A. tenuicollis and A. huronensis. Independently of a type of analysis and DNA region used, the topology of obtained trees was always identical; A. tenuicollis formed separate clade with A. huronensis forming a closely related sister group.

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Acknowledgments

M. O. greatly appreciates Dr. Xi Bing Wen (Freshwater Fisheries Research Centre, Wuxi, China) for invaluable help during material collection. This study was financially supported by the Grant Agency of the Slovak Republic (projects VEGA 2/0014/10 and 2/0129/12), by the Slovak Research and Development Agency under contract APVV-0653-11, by the Czech Science Foundation (project P505/12/G112), and by the Institute of Parasitology (RVO: 60077344). The study was realised as part of the project “Centre of Excellence for Parasitology” (Code ITMS: 26220120022), based on support of the Operational Programme “Research & Development” funded from the European Regional Development Fund (rate 0.1).

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Authors and Affiliations

  1. Institute of Parasitology, Slovak Academy of Sciences, Košice, Slovakia

    Ivica Králová-Hromadová, Eva Bazsalovicsová & Mikuláš Oros

  2. Biology Centre ASCR, Institute of Parasitology, and Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic

    Jan Štefka

  3. Department of Molecular Biology, Faculty of Natural Sciences, Comenius University, Bratislava, Slovakia

    Silvia Bokorová

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  1. Ivica Králová-Hromadová
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  2. Jan Štefka
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  5. Mikuláš Oros
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Correspondence to Ivica Králová-Hromadová.

Additional information

Note: Nucleotide sequence data reported in this paper are available in the GenBank™, EMBL and DDBJ databases under the accession numbers KC834609-KC834634.

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Suppl. 1

Cox1 gene tree obtained from *BEAST. Posterior probabilities are provided above clades. Species codes, country codes, haplotype numbering and individual codes follow that on Table 2. (PDF 8 kb)

Suppl. 2

ITS2 gene tree obtained from *BEAST. Posterior probabilities are provided above clades. Abbreviations of species and country codes and numbering of individuals/ITS2 codes are explained in Table 1. (PDF 8 kb)

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Králová-Hromadová, I., Štefka, J., Bazsalovicsová, E. et al. The tapeworm Atractolytocestus tenuicollis (Cestoda: Caryophyllidea)—a sister species or ancestor of an invasive A. huronensis?. Parasitol Res 112, 3379–3388 (2013). https://doi.org/10.1007/s00436-013-3516-y

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