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Morphological and molecular characterization of larval trematodes infecting the assassin snail genus Anentome in Thailand

Published online by Cambridge University Press:  27 July 2022

N. Chomchoei ,
T. Backeljau ,
B. Segers ,
C. Wongsawad ,
P. Butboonchoo  and
N. Nantarat Open the ORCID record for N. Nantarat [Opens in a new window]
N. Chomchoei
Affiliation:
Ph.D.'s Degree Program in Biodiversity and Ethnobiology (International Program), Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand Applied Parasitology Research Laboratory, Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
T. Backeljau
Affiliation:
Royal Belgian Institute of Natural Sciences (BopCo - Barcoding facility for organisms and tissues of policy concern), Vautierstraat 29, B-1000 Brussels, Belgium Evolutionary Ecology Group, University of Antwerp, Universiteitsplein 1, B-2610 Antwerp, Belgium
B. Segers
Affiliation:
Royal Belgian Institute of Natural Sciences (BopCo - Barcoding facility for organisms and tissues of policy concern), Vautierstraat 29, B-1000 Brussels, Belgium
C. Wongsawad
Affiliation:
Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand Applied Parasitology Research Laboratory, Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand Research Center in Bioresources for Agriculture, Industry and Medicine, Faculty of Science, Chiang Mai University, Chiang Mai, 50200, Thailand
P. Butboonchoo
Affiliation:
Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand Applied Parasitology Research Laboratory, Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand Research Center in Bioresources for Agriculture, Industry and Medicine, Faculty of Science, Chiang Mai University, Chiang Mai, 50200, Thailand
N. Nantarat*
Affiliation:
Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand Applied Parasitology Research Laboratory, Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand Research Center in Bioresources for Agriculture, Industry and Medicine, Faculty of Science, Chiang Mai University, Chiang Mai, 50200, Thailand
*
Author for correspondence: N. Nantarat, E-mail: [email protected]
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Abstract

The assassin snail genus Anentome is widespread in Southeast Asia, and is distributed all over the world via the aquarium trade. One species of genus Anentome, Anentome helena, is known to act as intermediate host of parasitic trematodes. This study investigates the taxonomic diversity of larval trematodes infecting A. helena and Anentome wykoffi in Thailand. Larval trematodes were identified by combining morphological and DNA sequence data (cytochrome c oxidase I and internal transcribed spacer 2). Species delimitation methods were used to explore larval trematode species boundaries. A total of 1107 specimens of Anentome sp. were collected from 25 localities in Thailand. Sixty-two specimens of A. helena (n = 33) and A. wykoffi (n = 29) were infected by zoogonid cercariae, heterophyid metacercariae and echinostome metacercariae, with an overall prevalence of 5.6% (62/1107) and population-level prevalences in the range of 0.0–22.3%. DNA sequence data confirmed that the larval trematodes belong to the families Echinostomatidae, Heterophyidae and Zoogonidae. As such, this is the first report of zoogonid cercariae and heterophyid metacercariae in A. helena, and echinostome metacercariae in A. wykoffi. Moreover, this study provides evidence of tentative species-level differentiation between Thai Echinostoma sp. and Cambodian Echinostoma mekongi, as well as within Echinostoma caproni, Echinostoma trivolvis and Echinostoma revolutum.

Keywords

Nassariidaecercariaemetacercariaephylogenetic treespecies delimitation
Type
Research Paper
Information
Journal of Helminthology , Volume 96 , 2022 , e52
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Abe, EM, Guan, W, Guo, YH, et al. (2018) Differentiating snail intermediate hosts of Schistosoma spp. using molecular approaches: fundamental to successful integrated control mechanism in Africa. Infectious Diseases of Poverty 7, 1–13.CrossRefGoogle ScholarPubMed
Akaike, H (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.CrossRefGoogle Scholar
Anucherngchai, S, Tejangkura, T and Chontananarth, T (2016) Epidemiological situation and molecular identification of cercarial stage in freshwater snails in Chao-Phraya Basin, Central Thailand. Asian Pacific Journal of Tropical Biomedicine 6, 539–545.CrossRefGoogle Scholar
Barber, KE, Mkoji, GM and Loker, ES (2000) PCR-RFLP analysis of the ITS2 region to identify Schistosoma haematobium and S. bovis from Kenya. American Journal of Tropical Medicine and Hygiene 62, 434–440.CrossRefGoogle ScholarPubMed
Barnett, LJ and Miller, TL (2018) Host specificity and ecology of digenean parasites of nassariid gastropods in Central Queensland, Australia, with comments on host-parasite associations of the Nassariidae. Yale Journal of Biology and Medicine 91, 361–374.Google ScholarPubMed
Barnett, LJ, Miller, TL and Cribb, TH (2014) A review of the currently recognised zoogonid cercariae, including the identification and emergence ecology of Cercaria capricornia XI (Digenea: Zoogonidae) from Nassarius olivaceus (Gastropoda: Nassariidae) in Central Queensland, Australia. Folia Parasitologica 61, 322–330.CrossRefGoogle ScholarPubMed
Bogan, A and Hanneman, EH (2013) A carnivorous aquatic gastropod in the pet trade in North America: the next threat to freshwater gastropods. Ellipsaria 15, 18–19.Google Scholar
Bowles, J, Blair, D and McManus, DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165–173.CrossRefGoogle ScholarPubMed
Brandt, RAM (1974) The non-marine aquatic Mollusca of Thailand. Archiv für Molluskenkunde 105, 1–423.Google Scholar
Brunner, FS and Eizaguirre, C (2016) Can environmental change affect host/parasite-mediated speciation? Zoology 119, 384–394.CrossRefGoogle ScholarPubMed
Butboonchoo, P, Wongsawad, C, Wongsawad, P and Chai, JY (2020) Morphology and molecular identification of Echinostoma revolutum and Echinostoma macrorchis in freshwater snails and experimental hamsters in upper northern Thailand. Korean Journal of Parasitology 58, 499–511.CrossRefGoogle ScholarPubMed
Caron, Y, Rondelaud, D and Losson, B (2008) The detection and quantification of a digenean infection in the snail host with special emphasis on Fasciola sp. Parasitology Research 103, 735–744.CrossRefGoogle ScholarPubMed
Chai, JY and Jung, BK (2019) Epidemiology of trematode infections: an update. Advances in Experimental Medicine and Biology 1154, 359–409.CrossRefGoogle ScholarPubMed
Chai, JY, Cho, J, Chang, T, Jung, BK and Sohn, WM (2020) Taxonomy of Echinostoma revolutum and 37-collar-spined Echinostoma spp.: a historical review. Korean Journal of Parasitology 58, 343–371.CrossRefGoogle ScholarPubMed
Chantima, K, Chai, JY and Wongsawad, C (2013) Echinostoma revolutum: freshwater snails as the second intermediate hosts in Chiang Mai, Thailand. Korean Journal of Parasitology 51, 183–189.CrossRefGoogle ScholarPubMed
Chantima, K, Suk-Ueng, K and Kampan, M (2018) Freshwater snail diversity in Mae Lao agricultural basin (Chiang Rai, Thailand) with a focus on larval trematode infections. Korean Journal of Parasitology 56, 247–257.CrossRefGoogle Scholar
Chomchoei, N, Wongsawad, C and Nantarat, N (2018) Investigation of cryptic diversity and occurrence of echinostome metacercariae infection in Anentome helena (von dem Busch, 1847). Asian Pacific Journal of Tropical Medicine 11, 590–596.Google Scholar
Chontananarth, T and Wongsawad, C (2013) Epidemiology of cercarial stage of trematodes in freshwater snails from Chiang Mai province, Thailand. Asian Pacific Journal of Tropical Biomedicine 3, 237–243.CrossRefGoogle Scholar
Choudhary, K, Ray, S, Pandey, KC and Agrawal, N (2019) Morphological and molecular characterization of six Indian Tetracotyle type metacercariae (Digenea: Strigeidae Railliet, 1919), using ribosomal and mitochondrial DNA. Parasitology International 70, 33–40.CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) JModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
Dodangeh, S, Daryani, A, Sharif, M, Gholami, S, Kialashaki, E, Moosazadeh, M and Sarvi, S (2019) Freshwater snails as the intermediate host of trematodes in Iran: a systematic review. Epidemiology and Health 41, 1–13.CrossRefGoogle ScholarPubMed
Dunghungzin, C and Chontananarth, T (2020) Prevalence of cercarial infections in freshwater snails and morphological and molecular identification and phylogenetic trends of trematodes. Asian Pacific Journal of Tropical Medicine 13, 439–447.Google Scholar
Frandsen, F and Christensen, NO (1984) An introductory guide to the identification of cercariae from African freshwater snails with special reference to cercariae of trematode species of medical and veterinary importance. Acta Tropica 41, 181–202.Google Scholar
Fujisawa, T and Barraclough, TG (2013) Delimiting species using single-locus data and the generalized mixed Yule coalescent approach: a revised method and evaluation on simulated data sets. Systematic Biology 62, 707–724.CrossRefGoogle ScholarPubMed
Galindo, LA, Puillandre, N and Utge, J (2016) The phylogeny and systematics of the Nassariidae revisited (Gastropoda: Buccinoidea). Molecular Phylogenetics and Evolution 99, 337–353.CrossRefGoogle Scholar
Gilardoni, C, Etchegoin, J, Cribb, T, Pina, S, Rodrigues, P, Diez, ME and Cremonte, F (2020) Cryptic speciation of the zoogonid digenean Diphterostomum flavum n. sp. Demonstrated by morphological and molecular data. Parasite 27, 1–11.CrossRefGoogle Scholar
Gordy, MA and Hanington, PC (2019) A fine-scale phylogenetic assessment of digenean trematodes in Central Alberta reveals we have yet to uncover their total diversity. Ecology and Evolution 9, 3153–3238.CrossRefGoogle ScholarPubMed
Guindon, S, Delsuc, F, Dufayard, JF and Gascuel, O (2009) Estimating maximum likelihood phylogenies with PhyML. Methods in Molecular Biology 537, 113–137.CrossRefGoogle ScholarPubMed
Hillis, DM and Bull, JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42, 182–192.CrossRefGoogle Scholar
IBM Corp (2013) IBM SPSS statistics for windows, version 20.0. Armonk, New York, IBM Corp.Google Scholar
Kanev, I, Fried, B and Radev, V (2009) Collar spine models in the genus Echinostoma (Trematoda: Echinostomatidae). Parasitology Research 105, 921–927.CrossRefGoogle Scholar
Keiser, J and Utzinger, J (2009) Food-borne trematodiases. Clinical Microbiology Reviews 22, 466–483.CrossRefGoogle ScholarPubMed
Krailas, D, Chotesaengsri, S, Dechruksa, W, Namchote, S, Chuanprasit, C, Veeravechsukij, N, Boonmekam, D and Koonchornboon, T (2012) Species diversity of aquatic mollusks and their cercarial infections; Khao Yai National Park, Thailand. The Journal of Tropical Medicine and Parasitology 35, 37–47.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Moore, J (2002) Parasites and the behavior of animals. New York, Oxford University Press, p. 326.Google Scholar
Ng, TH, Tan, SK, Wong, WH, Meier, R, Chan, SY, Tan, HH and Yao, DC (2016) Molluscs for sale: assessment of freshwater gastropods and bivalves in the ornamental pet trade. PLoS One 11, 1–23.CrossRefGoogle ScholarPubMed
Pérez-Ponce De León, G, Garciá-Varela, M, Pinacho-Pinacho, CD, Sereno-Uribe, AL and Poulin, R (2016) Species delimitation in trematodes using DNA sequences: middle-American Clinostomum as a case study. Parasitology 143, 1773–1789.CrossRefGoogle ScholarPubMed
Puillandre, N, Brouillet, S and Achaz, G (2021) ASAP: assemble species by automatic partitioning. Molecular Ecology Resources 21, 609–620.CrossRefGoogle ScholarPubMed
Rambaut, A (2010) FigTree v1.4.3. Available at http://tree.bio.ed.ac.uk/software/figtree/ (accessed 22 March 2022).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, 901–904.CrossRefGoogle ScholarPubMed
Ronquist, F, Teslenko, M, van der Mark, P, et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Saitou, N and Nei, M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 406–425.Google ScholarPubMed
San Mauro, D and Agorreta, A (2010) Molecular systematics: a synthesis of the common methods and the state of knowledge. Cellular and Molecular Biology Letters 15, 311–341.CrossRefGoogle ScholarPubMed
Schell, SC (1970) How to know the trematodes. Iowa, W.C. Brown Company, p. 355.Google Scholar
Scholz, T, Ditrich, O and Giboda, M (1991) Differential diagnosis of opisthorchiid and heterophyid metacercariae (Trematoda) infecting flesh of cyprinid fish from Nam Ngum Dam Lake in Laos. The Southeast Asian Journal of Tropical Medicine and Public Health 22, 171–173.Google ScholarPubMed
Srivathsan, A and Meier, R (2012) On the inappropriate use of Kimura-2-parameter (K2P) divergences in the DNA-barcoding literature. Cladistics 28, 190–194.CrossRefGoogle ScholarPubMed
Strong, EE, Galindo, LA and Kantor, YI (2017) Quid est Clea helena? Evidence for a previously unrecognized radiation of assassin snails (Gastropoda: Buccinoidea: Nassariidae). PeerJ 5, 1–41.CrossRefGoogle Scholar
Suchard, MA, Lemey, P, Baele, G, Ayres, DL, Drummond, AJ and Rambaut, A (2018) Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evolution 4, 1–5.CrossRefGoogle ScholarPubMed
Sullivan, J (2005) Maximum-likelihood methods for phylogeny estimation. Molecular Evolution: Producing the Biochemical Data 395, 757–779.Google ScholarPubMed
Swofford, DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sunderland, Massachusetts, Sinauer Associates.Google Scholar
Thaenkham, U, Phuphisut, O, Nuamtanong, S, et al. (2017) Genetic differences among Haplorchis taichui populations in Indochina revealed by mitochondrial COX1 sequences. Journal of Helminthology 91, 597–604.CrossRefGoogle ScholarPubMed
Thompson, JD, Higgins, DG and Gibson, TJ (1994) CLUSTAL w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Waikagul, J and Thaenkham, U (2014) Collection of fish-borne trematodes in infective stage from the fish: the second intermediate host. pp. 49–60 in Waikagul, J and Thaenkham, U (Eds) Approaches to research on the systematics of fish-borne Trematodes. Cambridge, Massachusetts, Academic Press.CrossRefGoogle Scholar
Wardle, WJ (1993) A new zoogonid cercaria (Trematoda: Digenea) from the Florida horse conch, Pleuroploca gigantea in the Northwestern Gulf of Mexico. Journal of the Helminthological Society of Washington 60, 216–218.Google Scholar
Wiroonpan, P, Chontananarth, T and Purivirojkul, W (2020) Cercarial trematodes in freshwater snails from Bangkok, Thailand: prevalence, morphological and molecular studies, and human parasite perspective. Parasitology 148, 366–383.CrossRefGoogle ScholarPubMed
Wongsawad, C, Nantarat, N and Wongsawad, P (2017) Phylogenetic analysis reveals cryptic species diversity within minute intestinal fluke, Stellantchasmus falcatus Onji and Nishio, 1916 (Trematoda, Heterophyidae). Asian Pacific Journal of Tropical Medicine 10, 165–170.CrossRefGoogle Scholar
Wongsawad, C, Nantarat, N, Wongsawad, P, Butboonchoo, P and Chai, JY (2019) Morphological and molecular identification of Stellantchasmus dermogenysi n. sp. (Digenea: Heterophyidae) in Thailand. Korean Journal of Parasitology 57, 257–264.CrossRefGoogle Scholar
Yutemsuk, N, Krailas, D, Anancharoenkit, C, Phanpeng, L and Dechruksa, W (2017) Trematode infections of freshwater snails genus Clea A. Adams, 1855 in the reservoir of lower northeast Thailand. Joint International Tropical Medicine Meeting 6, 7–16.Google Scholar
Zhang, J, Kapli, P, Pavlidis, P and Stamatakis, A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869–2876.CrossRefGoogle ScholarPubMed
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