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New record and phylogenetic assessment of Apopharynx bolodes (Braun, 1902) (Digenea: Psilostomidae), a parasite of Eurasian Coot Fulica atra Linnaeus, 1758 (Aves: Rallidae)

Published online by Cambridge University Press:  05 November 2024

S.A. Vlasenkov Open the ORCID record for S.A. Vlasenkov [Opens in a new window] ,
L.N. Akimova Open the ORCID record for L.N. Akimova [Opens in a new window]  and
S.G. Sokolov Open the ORCID record for S.G. Sokolov [Opens in a new window]
S.A. Vlasenkov
Affiliation:
A.N. Severtsov Institute of Ecology and Evolution, RAS, Leninsky Prospect 33, Moscow, 119071 Russia
L.N. Akimova
Affiliation:
State Research and Production Association “Scientific and Practical Center of the National Academy of Sciences of Belarus for Bioresources”, Akademicheskaya Street 27, Minsk, 220072, Belarus
S.G. Sokolov*
Affiliation:
A.N. Severtsov Institute of Ecology and Evolution, RAS, Leninsky Prospect 33, Moscow, 119071 Russia
*
Corresponding author: S.G. Sokolov; Email: [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Phylogenetic studies of aberrant species are of considerable scientific interest because their taxonomic rank in traditional systems based on morphological characters is not infrequently overestimated. Apopharynx bolodes (Braun, 1902) is one of the few psilostomid digeneans devoid of the pharynx. This is considered a sufficient basis for assigning it and similar species to the subfamily Apopharynginae. We found A. bolodes in Fulica atra Linnaeus, 1758 from Belarus, described it morphologically, and genotyped it by the 28S rRNA gene and the ITS2 region. It is the first molecular data on A. bolodes and the first record of this digenean species in Belarus. The phylogenetic analysis based on partial sequences of the 28S rRNA gene showed that A. bolodes is closely related to the Sphaeridiotrema spp. (Sphaeridiotrematinae). However, this phylogenetic inference has not received yet support with data on the ITS2 region.

Keywords

ApopharynginaeBelarusSphaeridiotrematinaetaxonomic structure
Type
Short Communication
Information
Journal of Helminthology , Volume 98 , 2024 , e65
Copyright
© The Author(s), 2024. Published by Cambridge University Press

Introduction

Eurasian Coot Fulica atra Linnaeus, 1758 is a wetland bird widespread in the Palearctic. Its diet may vary depending on habitat and season but is generally characterised by the predominance of aquatic plants over animal prey (Delić Reference Delić1990; Perrow et al. Reference Perrow, Schutten, Howes, Holzer, Madgewick and Jowitt1997; Mouronval et al. Reference Mouronval, Guillemain, Canny and Poirier2007; Metna et al. Reference Metna, Lardjane-Hamiti, Boukhemza-Zemmouri, Boukhemza, Merabet and Abba2015; Sakai Reference Sakai2015). This feeding pattern favours infection with psilostomid and notocotylid digeneans, whose larvae, adolescariae, encyst in the environment, often on aquatic plants, and are consumed by coots together with them.

The Psilostomidae is a relatively small family of the Echinostomatoidea, whose adults parasitise mainly wetland birds (Kostadinova Reference Kostadinova, Jones, Bray and Gibson2005; Tkach et al. Reference Tkach, Kudlai and Kostadinova2016; Kudlai et al. Reference Kudlai, Kostadinova, Pulis and Tkach2017). Taxonomic structure and composition of this family requires revision (Tkach et al. Reference Tkach, Kudlai and Kostadinova2016; Kudlai et al. Reference Kudlai, Pulis, Kostadinova and Tkach2016, Reference Kudlai, Kostadinova, Pulis and Tkach2017; Kalinina et al. Reference Kalinina, Tatonova and Besprozvannykh2022). To date, eight species of the Psilostomidae have been recorded in the Eurasian Coot: Apopharynx bolodes (Braun, Reference Braun1902), Psilochasmus oxyurus (Creplin, 1825), Psilostomum brevicolle (Creplin, 1829), Psilostomum fulicae Ricci & Carrescia, Reference Ricci and Carrescia1961, Psilotrema oligoon (von Linstow, 1887), Psilotrema simillimum (Mühling, 1898), Psilotrema spiculigerum (Mühling, 1898), and Sphaeridiotrema globulus (Rudolphi, 1819) (e.g. Pukhov Reference Pukhov1939; Bykhovskaya-Pavlovskaya Reference Bykhovskaya-Pavlovskaya1953; Ricci and Carrescia Reference Ricci and Carrescia1961; Macko Reference Macko1968; Filimonova & Shalyapina Reference Filimonova, Shalyapina, Ryzhikov and Folitarek1975; Iskova Reference Iskova and Sharpilo1985; Serbina Reference Serbina2006; Sitko et al. Reference Sitko, Faltýnková and Scholz2006; Niewiadomska Reference Niewiadomska2015). Four of them (P. brevicolle, P. simillimum, P. oxyurus, and S. globulus) have been studied using molecular methods, though all genotyped isolates were derived not from Eurasian Coot but from other hosts.

Of representatives of the Psilostomidae parasitising Eurasian Coot, A. bolodes is of a particular interest. It is the type and only species of Apopharynx Lühe, 1909, which, in turn, is the type genus of the Apopharynginae Yamaguti, Reference Yamaguti1958 (Yamaguti Reference Yamaguti1958, Reference Yamaguti1971; Kostadinova Reference Kostadinova, Jones, Bray and Gibson2005). The differentiating feature of this subfamily is the absence of the pharynx (Yamaguti, Reference Yamaguti1958, Reference Yamaguti1971; Byrd & Prestwood Reference Byrd and Prestwood1969; Kostadinova Reference Kostadinova, Jones, Bray and Gibson2005). In addition to the type genus, the Apopharynginae includes Psilotornus Byrd & Prestwood, Reference Byrd and Prestwood1969 (Byrd & Prestwood Reference Byrd and Prestwood1969; Yamaguti, Reference Yamaguti1971; Kostadinova Reference Kostadinova, Jones, Bray and Gibson2005), whose representatives, like A. bolodes, have not yet been genotyped either. Molecular data on this subfamily are much needed for the future revision of the Psilostomidae.

In this paper, we report the presence of A. bolodes in Eurasian Coot in Belarus and assess the phylogenetic position of this parasite species.

Materials and methods

Two adult specimens of A. bolodes were collected from the bursa of Fabricius during parasitological study of individuals of Eurasian Coot (n = 15) shot by licensed hunters at Lake Naroch near Naroch Village (Minsk Region), Belarus (54°54’8’’ N, 26°44’37’’ E), in September 2023. Digenean specimens were relaxed in fresh water, fixed with 70% ethanol, and, after a few minutes, transferred to 96% ethanol. These parasites have subsequently been studied by morphological and molecular techniques. For the morphological study, the specimens were stained with acetocarmine, dehydrated in a graded ethanol series, cleared with dimethyl phthalate, and finally mounted in Canada balsam. All the measurements are given in micrometres (μm). The drawings were made with the help of the camera lucida. Voucher specimens of A. bolodes (hologenophore and paragenophore) are stored in the personal collection of the first author.

DNA was extracted separately from small body fragments of two specimens of A. bolodes according to Holterman et al. (Reference Holterman, van der Wurff, van den Elsen, van Megen, Bongers, Holovachov, Bakker and Helder2006). BIO-RAD T100 Thermal Cycler amplified the fragments. Polymerase chain reactions were performed in a total volume of 25 μL using the Encyclo Plus PCRkit (Eurogene) according to the manufacturer’s instructions. Partial 28S rRNA gene sequences were amplified with ZX1aF (5′-ACCCGCTGAATT-TAAGCATAT-3′) (Palm et al. Reference Palm, Waeschenbach, Olson and Littlewood2009) and 1500R (5′-GCTATCCTGAGGGAAACTTCG-3′) (Tkach et al. Reference Tkach, Grabda-Kazubska, Pawlowski and Swiderski1999) primers. The following protocol was used: initial denaturation at 95 °C (5 min); 40 cycles of 30 s at 95 °C; 30 s at 55 °C; 2 min at 72 °C; and 7 min at 72 °C for the final extension. To amplify the complete sequences of the ITS2 region, we used 3S (5′-GTACCGGTGGATCACGTGGCTAGTG-3′) (Morgan & Blair, Reference Morgan and Blair1995) and ITS2.2 (5′-CCTGGTTAGTTTCTTTTCCTCCGC-3′) (Cribb et al., Reference Cribb, Adlard and Bray1998) primers, according to the following protocol: cycle 1 was 95 °C for 3 min, 45 °C for 2 min and 72 °C for 150 s; this was followed by four shorter cycles, 95 °C for 45 s, 50 °C for 45 s and 72 °C for 90 s, then a further 30 cycles of 95 °C for 20 s, 52 °C for 20 s, and 72 °C for 90 s and 5 min at 72 °C for the final extension. Unfortunately, amplicons could be obtained for only one specimen. All attempts to amplify markers of mithochondrial DNA (cox1 and nd1 genes) in A. bolodes using various primers were unsuccessful.

For the phylogenetic reconstructions of A. bolodes based on the 28S rRNA gene datasets, the newly obtained sequence was aligned with those of 22 psilostomid species available in GenBank NCBI (Table S1). Only sequences exceeding the length of 1000 bp were used for the 28S rRNA gene-based analysis. When we generated a tree based on complete sequences of the ITS2 region, the newly obtained sequence was aligned with those of the six psilostomid species from the NCBI GenBank (Table S1). The general alignments of partial sequences of 28S rRNA gene and complete sequences of ITS2 region were generated with “MAFFT” v7.520 (Katoh & Standley Reference Katoh and Standley2013) as implemented in Conda environment (Anaconda Software Distribution 2020), and then checked manually in SeaView Version 4.0 software (Gouy et al. Reference Gouy, Guindon and Gascuel2010). The evolutionary model was estimated with the help of jModeltest 2.1.7 (Darriba et al. Reference Darriba, Taboada, Doallo and Posada2012). The best fitted model was GTR+G+I for analysis based on the 28S rRNA gene dataset, and TVM+I model for analysis based on the ITS2 region dataset. Bayesian Inference analyses were performed in MrBayes 3.2.7a (Ronquist et al. Reference Ronquist, Teslenko, van der Mark, Ayres, Darling, Höhna, Larget, Liu, Suchard and Huelsenbeck2012) at CIPRES (Miller et al. Reference Miller, Pfeiffer and Schwartz2010) portal for 15,000,000 generations and the first 25% generations were discarded for burn-in. Representatives of the Notocotylidae were used as an outgroup following Kalinina et al. (Reference Kalinina, Tatonova and Besprozvannykh2022).

Results

Apopharynx bolodes (Braun, Reference Braun1902) (Figure 1). Description (based on one hologenophore and one paragenophore). Body fusiform, 1742–2309 long, with maximum width just anteriorly to midbody, at least 795–894 (right margin of body was cut off and used for DNA extraction). Tegument spinous. Forebody 37.6%–38.7% of body length. Oral sucker almost rounded, subterminal, 282–324 wide, mouth opens ventrally. Preoral lobe distinct. Ventral sucker almost rounded, 272–307 × 269–310. Sucker width ratio 1:0.95. Prepharynx and pharynx absent. Oesophagus 287–290 long. Intestinal bifurcation in third quarter of forebody or at border between third and posterior quarters of forebody. Caeca terminating blindly near posterior extremity of body. Testes two, tandem, smooth, partly overlapping; anterior testis rounded or almost so, 277–404 × 278–439, in anterior half of hindbody; posterior testis suboval, 295–367 × 241–280, in anterior half of hindbody. Post-testicular field 7.4%–8.6% of body length. Cirrus-sac elongate-oval, 242–376 × 115–116, anterior to ventral sucker. Internal seminal vesicle tubular, convoluted. Pars prostatica tubular when cirrus everted; surrounded by prostatic cells. Cirrus unarmed, oval in everted state. Common genital pore sinistro-submedian, between mid-level of oesophagus and intestinal bifurcation. Ovary rounded or almost so, 148–218 × 147–239, median or slightly dextro-submedian, pretesticular, contiguous with or partly overlapping anterior testis, contiguous with or posterior to posterior margin of ventral sucker. Laurer’s canal opens antero-sinistro-dorsally to ovary. Oötype with Mehlis’ gland antero-sinistral to ovary. Uterus pre-ovarian. Proximal part of uterus acts as uterine seminal vesicle; distal part terminates with sphincter, opens into genital atrium dorsally to male genital pore. Eggs deformed in balsam; length of least-deformed eggs 95. Vitellarium follicular; follicles in two lateral fields between intestinal bifurcation and posterior margin of posterior testis; not confluent. Vitelline reservoir at level of posterior margin of ovary. Excretory vesicle Y-shaped, with stem extending to posterior margin of posterior testis; pore terminal.

Figure 1. Hologenophore of Apopharynx bolodes from Fulica atra, Belarus. Scale bar, 800 μm.

In phylogenetic analysis based on partial 28S rRNA gene sequences, A. bolodes (GenBank NCBI accession number PP848221) was a weakly supported sister to the Sphaeridiotrema spp. clade, which was also weakly supported (Figure 2). In turn, A. bolodes+ Sphaeridiotrema spp. clade had a poorly supported sister relationship with the strongly supported P. oxyurus + P. brevicolle clade. The clade including all the species mentioned above was a strongly supported sister to the poorly supported clade, which was in turn subdivided into the poorly supported group containing Macracetabulum albeolae Kudlai, Kostadinova, Pulis & Tkach, Reference Kudlai, Kostadinova, Pulis and Tkach2017, Longisaccus elvirae Kudlai, Kostadinova, Pulis & Tkach, Reference Kudlai, Kostadinova, Pulis and Tkach2017, Byrdtrema sponsae Kudlai, Kostadinova, Pulis & Tkach, Reference Kudlai, Kostadinova, Pulis and Tkach2017 and Neopsilotrema spp. and the strongly supported group containing Psilotrema limosum Kalinina, Tatonova & Besprozvannykh, Reference Kalinina, Tatonova and Besprozvannykh2022 and unidentified psilostomids from the study of Schwelm et al. (Reference Schwelm, Kudlai, Smit, Selbach and Sures2020).

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

The phylogenetic tree based on complete sequences of the ITS2 region A. bolodes (GenBank NCBI accession number PQ164795) appeared as a weakly supported sister to Neopsilotrema spp. clade. The A. bolodes + Neopsilotrema spp. clade had the poorly supported sister relationship with Psilostomum brevicolle (Creplin, 1829). In turn, the clade of all these species formed the strongly supported sister relationship with Sphaeridiotrema pseudoglobulus McLaughlin, Scott & Huffman, 1993 (Figure 3).

Figure 3. Phylogenetic relationships of Apopharynx bolodes reconstructed by Bayesian Inference analysis of ITS2 region complete sequences. Posterior probability values lower than 0.9 are not shown. Newly obtained sequences are underlined.

Discussion

The trematode specimens examined in our study correspond to A. bolodes in all key morphological characters, namely, the body shape, the absence of the pharynx, the position of the ventral sucker, the common genital pore, the cirrus sac and the gonads, and the distribution of the vitelline follicles (Braun Reference Braun1902; Bykhovskaya-Pavlovskaya Reference Bykhovskaya-Pavlovskaya1953; Kostadinova Reference Kostadinova, Jones, Bray and Gibson2005). According to several authors, A. bolodes lacks not the pharynx but the oral sucker (Odhner Reference Odhner1913; Skrjabin Reference Skrjabin and Skrjabin1947; Odening Reference Odening1962). However, following the concept of Kostadinova (Reference Kostadinova, Jones, Bray and Gibson2005), we believe that this species is actually devoid of the pharynx. Dimensions of the body, organs, and eggs in our specimens are similar to those reported for this species by other authors (Table 1).

Table 1. Comparative characterisation of different isolates of Apopharynx bolodes based on some metric traits (in μm)

a Diameter.

This is the first report of A. bolodes from Belarus. This parasite species has previously been found in Kaliningrad, Novosibirsk, and Rostov regions of Russia (Braun Reference Braun1902; Pukhov Reference Pukhov1939; Bykhovskaya-Pavlovskaya Reference Bykhovskaya-Pavlovskaya1953; Filimonova & Shalyapina Reference Filimonova, Shalyapina, Ryzhikov and Folitarek1975; Serbina Reference Serbina2006), Hungary (Edelényi Reference Edelényi1974), Poland (Sulgostowska Reference Sulgostowska1960; Pojmańska et al. Reference Pojmańska, Machalska and Niewiadomska1984), Slovakia (Macko Reference Macko1968), and Germany (Odening Reference Odening1962). In all cases, this parasite was found only in Eurasian Coot. The life cycle of A. bolodes has not been elucidated.

We obtained the first data on the phylogenetic position of A. bolodes. The 28S- and ITS2-based phylogeny we obtained here are not consistent with each other. However, they are, in principle, difficult to compare because of the sharply different number of species included in the corresponding analyses. The position of A. bolodes on the 28S-tree as a sister taxon to the Sphaeridiotrema spp. clade is supported by morphological data. Members of these two clades are similar in body shape and the distribution of the vitelline follicles (compare with Bykhovskaya-Pavlovskaya Reference Bykhovskaya-Pavlovskaya1953; Kalinina et al. Reference Kalinina, Tatonova and Besprozvannykh2022). However, given the current results of the analysis of complete sequences of the ITS2 region, the close relationship of A. bolodes with the Sphaeridiotrema spp. clade requires additional molecular verification.

In traditional systems of the Psilostomidae, the aberrant morphology of A. bolodes and Psilotornus spp., that is, the absence of the pharynx, is considered a strong argument in favour of assigning them to a separate subfamily, the Apopharynginae (Yamaguti Reference Yamaguti1958, Reference Yamaguti1971; Kostadinova Reference Kostadinova, Jones, Bray and Gibson2005). However, this is the only argument supporting this hypothesis. The close phylogenetic affinity between A. bolodes and the Sphaeridiotrema spp. clade (Sphaeridiotrematinae Yamaguti, Reference Yamaguti1958) on the 28S-tree casts doubts on the necessity of assigning Apopharynx and Sphaeridiotrema Odhner, Reference Odhner1913 to different subfamilies.

All psilostomid species involved in our phylogenetic analysis based on the 28S rRNA gene dataset appeared to be distributed across three major clades, namely (i) P. limosum with Psilostomidae gen. sp. from Schwelm et al. (Reference Schwelm, Kudlai, Smit, Selbach and Sures2020), (ii) M. albeolae, L. elvirae, and B. sponsae with Neopsilotrema spp., and (iii) P. oxyurus, P. brevicolle, and A. bolodes with Sphaeridiotrema spp. These results are congruent with the clustering of psilostomids in Kalinina et al. (Reference Kalinina, Tatonova and Besprozvannykh2022). However, the support for the second and the third clades in our tree was much lower than in the tree of Kalinina et al. (Reference Kalinina, Tatonova and Besprozvannykh2022). The first of these main clades contains species of the Psilostominae Looss, 1900 (at least P. limosum), the second contains species of the Psilostominae and the Psilostomidae incertae sedis by Tkach et al. (Reference Tkach, Kudlai and Kostadinova2016), and the third contains species of the Psilostominae, the Apopharynginae, and the Sphaeridiotrematinae. Overall, our data, similarly to those of Kalinina et al. (Reference Kalinina, Tatonova and Besprozvannykh2022), support the conclusion of Kudlai et al. (Reference Kudlai, Kostadinova, Pulis and Tkach2017) that the current subdivision of the Psilostomidae into subfamilies probably does not reflect true phylogenetic relationships of the psilostomid genera. The observed distribution of diagnostic characters of the Psilostominae Looss, 1900 between three major clades (i–iii) (see Kudlai et al. Reference Kudlai, Kostadinova, Pulis and Tkach2017; Kalinina et al. Reference Kalinina, Tatonova and Besprozvannykh2022) seems to indicate that the subdivision of the Psilostomidae into subfamilies should be completely abandoned. However, a final decision on this issue should be postponed until the accumulation of more molecular data on psilostomids.

Supplementary material

The supplementary material for this article can be found at http://doi.org/10.1017/S0022149X24000543.

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 bird is a quarry species in Belarus, therefore ethical approval under the law of that country was not required.

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Figure 0

Figure 1. Hologenophore of Apopharynx bolodes from Fulica atra, Belarus. Scale bar, 800 μm.

Figure 1

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

Figure 2

Figure 3. Phylogenetic relationships of Apopharynx bolodes reconstructed by Bayesian Inference analysis of ITS2 region complete sequences. Posterior probability values lower than 0.9 are not shown. Newly obtained sequences are underlined.

Figure 3

Table 1. Comparative characterisation of different isolates of Apopharynx bolodes based on some metric traits (in μm)

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