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Phylogenetic position of Ancyrocephalus (sensu lato) curtus Achmerov, 1952 (Monopisthocotylea, Dactylogyridae), a parasite of fish Perccottus glenii Dybowski, 1877(Gobiiformes: Odontobutidae)

Published online by Cambridge University Press:  06 May 2024

Sergey G. Sokolov Open the ORCID record for Sergey G. Sokolov [Opens in a new window] ,
Fuat K. Khasanov Open the ORCID record for Fuat K. Khasanov [Opens in a new window]  and
Sergei A. Vlasenkov Open the ORCID record for Sergei A. Vlasenkov [Opens in a new window]
Sergey G. Sokolov
Affiliation:
A.N. Severtsov Institute of Ecology and Evolution, RAS, Leninsky Prospect 33, Moscow, 119071 Russia
Fuat K. Khasanov
Affiliation:
A.N. Severtsov Institute of Ecology and Evolution, RAS, Leninsky Prospect 33, Moscow, 119071 Russia
Sergei A. Vlasenkov*
Affiliation:
A.N. Severtsov Institute of Ecology and Evolution, RAS, Leninsky Prospect 33, Moscow, 119071 Russia
*
Corresponding author: Sergei A. Vlasenkov; Email: svlasenkov22@gmail.com
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Abstract

The genus Ancyrocephalus sensu lato is a large assemblage of species of dactylogyrid monopisthocotyleans without clear taxonomic boundaries. Despite an urgent need for revision, only three representatives of this taxon have been molecularly characterised so far. We found specimens of Ancyrocephalus curtus, a previously non-genotyped species, in gills of Perccottus glenii caught in the River Syumnyur, Amur Basin, Russia. The aim of this study was to assess the phylogenetic position of this parasite using partial sequences of 28S rRNA gene. In the phylogenetic tree, A. curtus appeared as a sister taxon to the dactylogyrine genus Gobioecetes. The new molecular evidence supports the hypothesis about the non-monophyletic status of Ancyrocephalus sensu lato.

Keywords

28S rDNAAmur basinmonogeneanpolyphyly
Type
Short Communication
Information
Journal of Helminthology , Volume 98 , 2024 , e37
Copyright
© The Author(s), 2024. Published by Cambridge University Press

Introduction

Ancyrocephalus Creplin, 1839, a large assemblage of dactylogyrid monopisthocotyleans, is a taxonomically problematic genus (Bychowsky and Nagibina Reference Bychowsky and Nagibina1970; Kritsky and Nitta, Reference Kritsky and Nitta2019; Kmentová et al. Reference Kmentová, Cruz-Laufer, Pariselle, Smeets, Artois and Vanhove2022). The number of species attributed to it has diminished after numerous revisions (e.g., Bychowsky and Nagibina Reference Bychowsky and Nagibina1970; Beverley-Burton Reference Beverley-Burton, Margolis and Kabata1984; Dossou and Euzet Reference Dossou and Euzet1984; Agarwal et al. Reference Agarwal, Yadav and Kritsky2001; Kritsky et al. Reference Kritsky, Pandey, Agrawal and Abdullah2004; Dmitrieva et al. Reference Dmitrieva, Gerasev, Gibson, Pronkina and Galli2012; Kmentová et al. Reference Kmentová, van Steenberge, Raeymaekers, Koblmüller, Hablützel, Bukinga, N’sibula, Mulungula, Nzigidahera, Ntakimazi, Gelnar and Vanhove2018; Kritsky and Nitta Reference Kritsky and Nitta2019). Nevertheless, the concept of Ancyrocephalus sensu lato is still applicable to 39 nominal dactylogyrid species with four anchors connected with dorsal and ventral bars and seven pairs of similar or different hooks (WoRMS 2024).

Molecular data are available only on three species of Ancyrocephalus sensu lato: Ancyrocephalus paradoxus Creplin, 1839, Ancyrocephalus percae Ergens, 1966, and Ancyrocephalus mogurndae (Yamaguti, 1940). Phylogenetic analyses based on these data have shown that Ancyrocephalus sensu stricto, as proposed by Bychowsky and Nagibina (Reference Bychowsky and Nagibina1970) for A. paradoxus (type) and A. percae from freshwater Palaearctic percid fishes, appears to be a natural taxon (Mathews et al. Reference Mathews, Domingues, Maia, Silva, Adriano and Aguiar2021; Kmentová et al. Reference Kmentová, Cruz-Laufer, Pariselle, Smeets, Artois and Vanhove2022; Osaki-Pereira et al. Reference Osaki-Pereira, Narciso, Vieira, Müller, Ebert and da Silva2023). At the same time, A. mogurndae clusters with representatives of Eutrianchoratus Paperna, 1969, Gobioecetes Ogawa & Ito, Reference Ogawa and Itoh2017 , Heteronchocleidus Bychowsky, 1957, Pseudodactylogyrus Gussev, 1965, and Trianchoratus Price & Berry, 1966, confirming the polyphyly of Ancyrocephalus sensu lato (Wu et al. Reference Wu, Zhu, Xie and Li2006; Mendoza-Palmero et al. Reference Mendoza-Palmero, Blasco-Costa and Scholz2015; Kmentová et al. Reference Kmentová, Cruz-Laufer, Pariselle, Smeets, Artois and Vanhove2022). According to Kmentová et al. (Reference Kmentová, Cruz-Laufer, Pariselle, Smeets, Artois and Vanhove2022), A. mogurndae diverged from A. paradoxus and A. percae at the subfamily level: Dactylogyrinae vs Ancyrocephalinae.

Ancyrocephalus curtus Achmerov, 1952 is a host-specific gill-associated parasite of the odontobutid fish Perccottus glenii Dybowski, 1877. This fish is an invasive species with a rather small heartland (the Middle and the Lower Amur and several neighbouring water systems) and an extensive invader range (water bodies of Europe and Siberia) (Reshetnikov Reference Reshetnikov2010). Ancyrocephalus curtus has been recorded only in native populations of P. glenii and in some introduced populations confined to water bodies within the Upper Amur Basin (Sokolov and Frolov Reference Sokolov and Frolov2012; Sokolov et al. Reference Sokolov2013, Reference Sokolov, Reshetnikov and Protasova2014; Sokolov and Reshetnikov Reference Sokolov and Reshetnikov2020). The type locality of this parasite is Lake Bolon, Amur Basin (Akhmerov Reference Akhmerov1952). Here we provide the first phylogenetic assessment of A. curtus using partial sequences of 28S rRNA gene.

Material and methods

In July 2023, specimens of A. curtus (Figure 1) were collected from the gills of P. glenii caught in the River Syumnyur, a tributary of Lake Bolon, Amur Basin (49°52’56’’ N; 136°7’52’’ E). The parasites were fixed in 96% ethanol and stored at −18ºC. The parasite species was identified according to Akhmerov (Reference Akhmerov1952), Gussev (Reference Gussev1955), and Gussev et al. (Reference Gussev, Gerasev, Pugachev, Galli, Pugachev and Kritsky2009).

Figure 1. Ancyrocephalus curtus from Perccottus glenii. A – haptoral hard parts. B – male copulatory organ. d – dorsal anchors and dorsal haptoral bar; pn – penis; pt –accessory piece; v – ventral anchors and ventral haptoral bar. Scale bar; A, B = 20 μm.

Total DNA was extracted separately from small body fragments (anterior ends cut off at the level of eyespots) of two specimens according to Holterman et al. (Reference Holterman, van der Wurff, van den Elsen, van Megen, Bongers, Holovachov, Bakker and Helder2006). The remaining body parts of these specimens were treated with proteinase-K to soften the tissue and were mounted in glycerol-gelatine to study sclerotised structures. The extracted DNA was used as a template in the PCR reaction to amplify the partial D1–D2 domain of the 28S rRNA gene using forward C1 (5’-ACCCGCTGAATTTAAGCAT-3’) (Gouÿ de Bellocq et al. Reference Gouÿde Bellocq, Ferté, Depaquit, Justine, Tillier and Durette-Desset2001 ) and reverse primers D2 (5’- TGGTCCGTGTTTCAAGAC-3’) (Lê et al. Reference Lê, Lecointre and Perasso1993). Cycling conditions were as follows: 2 min at 94°C, 35 cycles of 1 min at 94°C, 1 min at 55°C, 1 min at 72°C, and a final extension for 10 min at 72°C. PCR products were examined on 1% agarose gels, stained with ethidium bromide, and photographed upon transillumination.

To assess the phylogenetic relationships of A. curtus, Bayesian Inference analyses based on partial sequences of 28S rRNA gene were performed. BLAST searches performed on newly obtained sequences demonstrated the highest matching with the sequences of members of the Dactylogyrinae sensu Kmentová et al. (Reference Kmentová, Cruz-Laufer, Pariselle, Smeets, Artois and Vanhove2022). For the phylogenetic reconstructions, newly obtained sequences were aligned with sequences of dactylogyrinines and some ancyrocephalines (only A. percae and A. paradoxus) available in the GenBank dataset. Alignments were performed using the Muscle algorithm (Edgar Reference Edgar2004) as implemented in SeaView Version 4.0 (Gouy et al. Reference Gouy, Guindon and Gascuel2010), after which the alignment was adjusted manually. The final length of the alignment was 606 bp. Bayesian algorithm was performed in MrBayes 3.2.7a (Ronquist et al. Reference Ronquist, Teslenko, van der Mark, Ayres, Darling, Höhna, Larget, Liu, Suchard and Huelsenbeck2012) with the GTR+G+I model. The evolutionary model was estimated with the help of jModeltest 2.1.7 (Darriba et al. Reference Darriba, Taboada, Doallo and Posada2012). In the analysis, 15,000,000 generations of the Markov chain Monte Carlo were simulated, and the selection was performed once every 100 generations. Three species of the Diplectanidae (i.e., Dolicirroplectanum lacustre Kmentová, Gelnar & Vanhove, 2021, Paradiplectanum sillagonum (Tripathi, 1959), and Pseudorhabdosynochus grouperi (Bu, Leong, Wong, Woo & Foo, 1999)) were used as outgroup (Kmentová et al. Reference Kmentová, Cruz-Laufer, Pariselle, Smeets, Artois and Vanhove2022).

Results

The two newly obtained sequences of 28S rRNA gene of A. curtus were identical. Bayesian Inference analysis showed that A. curtus was a strongly supported sister taxon to Gobioecetes (Figure 2). In turn, the A. curtus + Gobioecetes clade appeared as a strongly supported sister taxon to A. mogurndae, and this entire species group was nested in the highly supported clade, which also contained Eutrianchoratus cleithrium Lim, Reference Lim1989 , Heteronchocleidus buschkieli Bychowsky, 1957, Pseudodactylogyrus spp., and Trianchoratus gussevi Lim, Reference Lim1986. The above-mentioned representatives of Eutrianchoratus, Heteronchocleidus, and Trianchoratus formed a clade that had a strongly supported sister relationship to the A. mogurndae + (A. curtus + Gobioecetes) clade. Pseudodactylogyrus spp. occupied a basal position to all the species mentioned above.

Figure 2. Phylogenetic relationships of Ancyrocephalus curtus reconstructed by Bayesian Inference analysis of 28S rRNA gene sequences. Posterior probability values lower than 0.9 are not shown. Newly obtained sequences are underlined.

The clade containing A. mogurndae, A. curtus, Gobioecetes spp., Pseudodactylogyrus spp., and representatives of Eutrianchoratus, Heteronchocleidus, and Trianchoratus was resolved within the large, strongly supported Dactylogyrinae clade.

Discussion

In this study, we assessed the phylogenetic position of A. curtus from the type-host and the locality very close to the type-locality using molecular data. Our phylogenetic analysis shows that A. curtus shares the most recent common ancestor with the clade formed by Gobioecetes spp. from Japanese freshwater gobiid fish. The similarities between A. curtus and Gobioecetes spp. are evident in the morphology of the sclerotised male copulatory organ and the absence of the vaginal armament. These parasite species have a penis shaped as a long, coiled and/or sinuous tube with a conspicuous inflation at the base, and an accessory piece shaped as a separate, distinctly concaved plate, which is not connected to the proximal end of the penis (Gussev Reference Gussev1955; Ogawa and Itoh Reference Ogawa and Itoh2017; Nitta and Nagasawa Reference Nitta and Nagasawa2020). The most pronounced differences between A. curtus and Gobioecetes spp. are associated with the haptoral armatures. The former species has both the dorsal and the ventral haptoral bar, whereas Gobioecetes spp. have only the ventral bar (Gussev Reference Gussev1955; Ogawa and Itoh Reference Ogawa and Itoh2017; Nitta and Nagasawa Reference Nitta and Nagasawa2020).

Our findings suggest that there is no direct phylogenetic relationship between A. curtus and A. mogurndae. However, this conclusion is provisional because the identification of A. mogurndae specimens for which molecular data are available is not supported by any morphological evidence. Ancyrocephalus mogurndae is characterised by the same morphological type of the male copulatory organ as A. curtus and Gobioecetes spp. (Gussev Reference Gussev1955; Ogawa and Itoh Reference Ogawa and Itoh2017; Nitta and Nagasawa Reference Nitta and Nagasawa2020). At the same time, this species differs sharply from A. curtus and Gobioecetes spp. in the presence of the vaginal armament (Gussev Reference Gussev1955; Ogawa and Itoh Reference Ogawa and Itoh2017; Nitta and Nagasawa Reference Nitta and Nagasawa2020). Based on morphological and ecological data, Gerasev (Reference Gerasev2008) hypothesised that the group within Ancyrocephalus sensu lato containing A. curtus and A. mogurndae might have a monophyletic status. However, our results do not support this hypothesis.

The clade of A. mogurndae, A. curtus, and Gobioecetes spp. appeared as a member of a monophyletic group within the Dactylogyrinae, which also comprised Pseudodactylogyrus spp. and representatives of Eutrianchoratus, Heteronchocleidus, and Trianchoratus. Kmentová et al. (Reference Kmentová, Cruz-Laufer, Pariselle, Smeets, Artois and Vanhove2022) proposed to name this group Clade A9. Morphological synapomorphies for Clade A9 are not obvious. The only clearly distinctive feature of its members is that their range (or its native part, in case of invasive Pseudodactylogyrus spp.) lies within the Far Eastern and/or South-Eastern regions of Asia (Gussev Reference Gussev1955; Lim Reference Lim1986, Reference Lim1989; Buchmann et al. Reference Buchmann, Mellergaard and Køie1987).

The position of A. mogurndae and A. curtus on our tree combined with morphological differences between them and Gobioecetes spp. probably indicates that each of these representatives of Ancyrocephalus sensu lato should be assigned to a separate genus. However, we refrain from this taxonomic act until molecular data on other Ancyrocephalus spp. from the fishes of the Amur Basin described by Akhmerov (Reference Akhmerov1952) and Gussev (Reference Gussev1955) become available.

Acknowledgements

We sincerely thank Dr. E. Frolov and the staff of the United Directorate of State Natural Reserves and National Parks ‘Zapovednoe Priamurye’, and personally, Dr. R. Andronova and Mr. E. Mishakov for their assistance in organising field work.

Financial support

The work was partly funded by the Russian Ministry of Science and Higher Education FFER-2021-0005.

Competing interest

The authors declare that they have no competing interest.

Ethical standard

Not applicable. The host fish is an object of recreational fishing, and therefore, no ethics permit was required under the Russian law.

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Figure 0

Figure 1. Ancyrocephalus curtus from Perccottus glenii.A – haptoral hard parts. B – male copulatory organ. d – dorsal anchors and dorsal haptoral bar; pn – penis; pt –accessory piece; v – ventral anchors and ventral haptoral bar. Scale bar; A, B = 20 μm.

Figure 1

Figure 2. Phylogenetic relationships of Ancyrocephalus curtus reconstructed by Bayesian Inference analysis of 28S rRNA gene sequences. Posterior probability values lower than 0.9 are not shown. Newly obtained sequences are underlined.