Abstract
Purpose
The molecular profile of Pararhadinorhynchus magnus Ha, Amin, Ngo, Heckmann, 2018 described from Scatophagus argus (Linn.) off Haiphong in the Gulf of Tonkin, Pacific Ocean, Vietnam is provided for the first time. It was morphologically distinguished from the South Australian species, Pararhadinorhynchus mugilis Johnston and Edmonds, 1947 and Pararhadinorhynchus coorongensis Edmonds, 1973 from mullets. Two other species of Pararhadinorhynchus are also recognized: Pararhadinorhynchus upenei Wang, Wang, Wu, 1993 from China and Pararhadinorhynchus sodwanensis Lisitsyna, Kudlai, Cribb and Smit, 2019 from South Africa. The assignment of Diplosentis manteri Gupta and Fatma, 1980 to Pararhadinorhynchus is not recognized.
Methods
Sequences of the 18S, small internal transcribed spacers (ITS1-5.8S-ITS2) and 28S from nuclear DNA were generated to molecularly characterize P. magnus. The phylogenetic analyses were achieved by comparison of the 18S and ITS1-5.8S-ITS2 region only as the 28S amplified a short region (425–428 bp) that was not sufficient for the present study.
Results
Phylogenetic analyses showed that P. magnus and the other species of Pararhadinorhynchus sequenced were nested within separate clades in the case of 18S gene and suggesting that these species do not share a common ancestor. In contrast, the ITS1-5.8S-ITS2 region shows a close arrangement of species of Pararhadinorhynchus with molecular affinities to the family Diplosentidae, suggesting that final placement of these species in Transvenidae needs further study and revision.
Conclusions
The molecular data from the present study will provide further comparative insights into species of Pararhadinorhynchus and its close affiliation to other acanthocephalan species and genera from different geographical areas.
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References
Amin OM (2013) Classification of the Acanthocephala. Folia Parasitol 60:273–305
Amin OM, Chaudhary A, Heckmann R, Ha NV, Singh HS (2019) Redescription and molecular analysis of Neoechinorhynchus (Neoechinorhynchus) johnii Yamaguti, 1939 (Acanthocephala, Neoechinorhynchidae) from the Pacific Ocean off Vietnam. Parasite 26:43. https://doi.org/10.1051/parasite/2019041
Amin OM, Heckman RA, Ali AH (2018) The finding of Pacific transvenid acanthocephalans in the Arabian Gulf with the description of Paratrajectura longcementglandatus n. gen., n. sp. from perciform fishes and emendation of Transvenidae. J Parasitol 104:39–50. https://doi.org/10.1645/17-84
Amin OM, Heckman RA, Dallarés S, Constenla M, Ha NV (2019) Morphological and molecular description of Rhadinorhynchus laterospinosus Amin, Heckmann & Ha, 2011 (Acanthocephala, Rhadinorhynchidae) from marine fish off the Pacific coast of Vietnam. Parasite 26:14. https://doi.org/10.1051/parasite/2019015
Amin OM, Heckman RA, Dallarés S, Constenla M, Ha NV (2020) Morphological and molecular description of Rhadinorhynchus hiansi Soota and Bhattacharya, 1981 (Acanthocephala: Rhadinorhynchidae) from marine fish off the Pacific coast of Vietnam. J Parasitol 106:56–70
Arizono N, Kuramochi T, Kagei N (2012) Molecular and histological identification of the acanthocephalan Bolbosoma cf. capitatum from the human small intestine. Parasitol Int 61:715–718. https://doi.org/10.1016/j.parint.2012.05.011
Braicovich PE, Lanfranchi AL, Farber MD, Marvaldi AE, Luque JL, Timi JT (2014) Genetic and morphological evidence reveals the existence of a new family, genus and species of Echinorhynchida (Acanthocephala). Folia Parasitol 61:377–384
Edmonds SJ (1973) Australian Acanthocephala No. 14. On two species of Pararhadinorhynchus, one new. Trans R Soc Aust 97:19–21
Fonseca MCGD, Knoff M, Felizardo NN, Torres EJL, Di Azevedo MIN, Gomes DC, Clemente SCS, Iñiguez AM (2019) Acanthocephalan parasites of the flounder species Paralichthys isosceles, Paralichthy spatagonicus and Xystreurys rasile from Brazil. Rev Bras Parasitol Vet 28:346–359. https://doi.org/10.1590/s1984-29612019031
Galazzo DE, Dayanandan S, Marcogliese DJ, McLaughlin JD (2002) Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA-sequence data and comparisons with European congeners. Can J Zool 80:2207–2217. https://doi.org/10.1139/Z02-198
García-Varela M, Aznar FJ, Nadler SA (2009) Systematic position of Pseudocorynosoma and Andracantha (Acanthocephala, Polymorphidae) based on nuclear and mitochondrial gene sequences. J Parasitol 95:178–185. https://doi.org/10.1645/GE-1538.1
García-Varela M, Pérez-Ponce de León G, Aznar FJ, Nadler SA (2011) Ibirhynchus dimorpha n. gen. (Acanthocephala: Polymorphidae), inferred through morphological, ecological and molecular data. J Parasitol 97:97–105. https://doi.org/10.1645/GE-2350.1
García-Varela M, Pérez-Ponce de Leon G, de la Torre P, Cummings MP, Sarma SS, Laclette JP (2000) Phylogenetic relationships of Acanthocephala based on analysis of 18S ribosomal RNA gene sequences. J Mol Evol 50:532–540. https://doi.org/10.1007/s002390010056
García-Varela M, Mendoza-Garfias B, Choudhury A, Pérez-Ponce de León G (2017) Morphological and molecular data for a new species of Pomphorhynchus Monticelli, 1905 (Acanthocephala: Pomphorhynchidae) in the Mexican redhorse Moxostoma austrinum Bean (Cypriniformes: Catostomidae) in central Mexico. Syst Parasitol 94:989–1006. https://doi.org/10.1007/s11230-017-9756-y
García-Varela M, Nadler SA (2005) Phylogenetic relationships of Palaeacantocephala (Acanthocephala) inferred from SSU and LSU rDNA gene sequences. J Parasitol 91:1401–1409. https://doi.org/10.1645/GE-523R.1
García-Varela M, Pérez-Ponce de León G, Aznar FJ, Nadler SA (2013) Phylogenetic relationship among genera of Polymorphidae (Acanthocephala), inferred from nuclear and mitochondrial gene sequences. Mol Phylogenet Evol 68:176–184. https://doi.org/10.1016/j.ympev.2013.03.029
Giribet G, Sorensen MV, Funch P, Kristensen RM, Sterrer W (2004) Investigations into the phylogenetic position of Micrognathozoa using four molecular loci. Cladistics 20:1–13. https://doi.org/10.1111/j.1096-0031.2004.00004.x
Golvan YJ (1969) Systématique des Acanthocéphales (Acanthocephala Rudolphi, 1801). Première Partie. L’Ordre des Palaeacanthocephala Meyer, 1931. Premier fascicule. La Superfamille des Echinorhynchoidae (Cobbold, 1876) Golvan et Houin, 1963. Mém Muséum Natl Hist Nat 57:1–373
Gregori M, Aznar FJ, Abollo E, Roura A, González AF, Pascual S (2013) Nyctiphanes couchii as intermediate host for Rhadinorhynchus sp. (Acanthocephala, Echinorhynchidae) from NW Iberian Peninsula waters. Dis Aquat Org 105:9–20. https://doi.org/10.3354/dao02611
Ha NV, Amin OM, Ngo HD, Heckmann RA (2018) Descriptions of acanthocephalans, Cathayacanthus spinitruncatus (Rhadinorhynchidae) male and Pararhadinorhynchus magnus n. sp. (Diplosentidae), from marine fish of Vietnam, with notes on Heterosentis holospinus (Arhythmacanthidae). Parasite 25:35. https://doi.org/10.1051/parasite/2018032
Herlyn H, Piskurek O, Schmitz J, Ehlers U, Zischlera H (2003) The syndermatan phylogeny and the evolution of acanthocephalan endoparasitism as inferred from 18S rDNA sequences. Mol Phylogenet Evol 26:155–164. https://doi.org/10.1016/s1055-7903(02)00309-3
Johnston TH, Edmonds SJ (1947) Australian Acanthocephala No. 5. Trans R Soc Aust 71:13–19
Kráľová-Hromadová I, Tietz DF, Shinn AP, Špakulová V (2003) ITS rDNA sequences of Pomphorhynchus laevis (Zoega in Müller, 1776) and P. lucyi William & Rogers, 1984 (Acanthocephala: Palaeacanthocephala). Syst Parasitol 56:141–145. https://doi.org/10.1023/a:1026127219358
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Li L, Chen HX, Amin OM, Yang Y (2017) Morphological variability and molecular characterization of Pomphorhynchus zhoushanensis sp. nov. (Acanthocephala: Pomphorhynchidae), with comments on the systematic status of Pomphorhynchus Monticelli, 1905. Parasitol Int 66:693–698. https://doi.org/10.1016/j.parint.2017.05.010
Li L, Chen HX, Yang Y (2018) Morphological and molecular study of Neorhadinorhynchus nudus (Harada, 1938) (Acanthocephala: Cavisomidae) from Auxis thazard Lacepede (Perciformes: Scombridae) in the South China Sea. Acta Parasitol 63:479–485. https://doi.org/10.1515/ap-2018-0057
Lisitsyna OI, Kudlai O, Spraker TR, Tkach VV, Smales LR, Kuzmina TA (2019) Morphological and molecular evidence for synonymy of Corynosoma obtuscens Lincicome, 1943 with Corynosoma austral Johnston, 1937 (Acanthocephala: Polymorphidae). Syst Parasitol 96:105–110. https://doi.org/10.1007/s11230-018-9830-0
Lisitsyna OI, Kudlai O, Cribb TH, Smit NJ (2019) Three new species of acanthocephalans (Palaeacanthocephala) from marine fishes collected off the East Coast of South Africa. Folia Parasitol 66:012. https://doi.org/10.14411/fp.2019.012
Littlewood DTJ, Curini-Galletti M, Herniou EA (2000) The interrelationships of Proseriata (Platyhelminthes: seriata) flatworms tested with molecules and morphology. Mol Phylogenet Evol 16:449–466. https://doi.org/10.1006/mpev.2000.0802
Littlewood DTJ, Olson PD (2001) Small subunit rDNA and the phylum platyhelminthes: signal, noise, conflict and compromise. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the platyhelminthes. Taylor and Francis, London, pp 262–278
Martínez-Aquino A, Reyna-Fabián ME, Rosas-Valdez R, Razo-Mendivil U, de León GP, García-Varela M (2009) Detecting a complex of cryptic species within Neoechinorhynchus golvani (Acanthocephala: Neoechinorhynchidae) inferred from ITSs and LSU rDNA gene sequences. J Parasitol 95:1040–1047. https://doi.org/10.1645/GE-1926.1
Milne I, Lindner D, Bayer M, Husmeier D, McGuire G, Marshall DF, Wright F (2009) TOPALiv2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics 25:126–127. https://doi.org/10.1093/bioinformatics/btn575
Monks S (2001) Phylogeny of the Acanthocephala based on morphological characters. Syst Parasitol 48:81–115. https://doi.org/10.1023/A:1006400207434
Nakao M (2016) Pseudoacanthocephalus toshimai sp. nov. (Palaeacanthocephala: Echinorhynchidae), a common acanthocephalan of anuran and urodelan amphibians in Hokkaido, Japan, with a finding of its intermediate host. Parasitol Int 65:323–332. https://doi.org/10.1016/j.parint.2016.03.011
Near JT, Garey JR, Nadler SA (1998) Phylogenetic relationships of the acanthocephala inferred from 18S ribosomal DNA sequences. Mol Phylogenet Evol 10:287–298. https://doi.org/10.1006/mpev.1998.0569
Perrot-Minnot MJ (2004) Larval morphology, genetic divergence, and contrasting levels of host manipulation between forms of Pomphorhynchus laevis (Acanthocephala). Int J Parasitol 34:45–54. https://doi.org/10.1016/j.ijpara.2003.10.005
Pichelin S, Cribb TH (2001) The status of the Diplosentidae (Acanthocephala: Palaeacanthocephala) and a new family of acanthocephalans from Australian wrasses (Pisces: Labridae). Folia Parasitol 48:289–303. https://doi.org/10.14411/fp.2001.047
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256. https://doi.org/10.1093/molbev/msn083
Smales LR, Adlard RD, Elliot A, Kelly E, Lymbery AJ, Miller TL, Shamsi S (2018) A review of the Acanthocephala parasitising freshwater fishes in Australia. Parasitology 145:249–259. https://doi.org/10.1017/S0031182017001627
Sobecka E, Szostakowska B, MacKenzie K, Hemmingsen W, Prajsnar S, Eydal M (2012) Genetic and morphological variation in Echinorhynchus gadi Zoega in Müller, 1776 (Acanthocephala: Echinorhynchidae) from Atlantic cod Gadus morhua L. J Helminthol 86:16–25. https://doi.org/10.1017/S0022149X10000891
Steinauer ML, Garcia-Vedrenne AE, Weinstein SB, Kuris AM (2019) Acanthocephalan parasites of the oarfish, Regale cusrusselii (Regalecidae), with a description of a new species of Gymnorhadinorhynchus (Acanthocephala: Gymnorhadinorhynchidae). J Parasitol 105:124–132. https://doi.org/10.1645/17-53
Thompson JD, Higgins DG, 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 Res 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673
Tkach VV, Lisitsyna OI, Crossley JL, Binh TT, Bush SE (2013) Morphological and molecular differentiation of two new species of Pseudoacanthocephalus Petrochenko, 1958 (Acanthocephala: Echinorhynchidae) from amphibians and reptiles in the Philippines, with identification key for the genus. Syst Parasitol 85:11–26. https://doi.org/10.1007/s11230-013-9409-8
Vardić Smrzlić I, Valić D, Kapetanović D, Filipović Marijić V, Gjurčević E, Teskeredžić E (2015) Pomphorhynchus laevis (Acanthocephala) from the Sava River basin: new insights into strain formation, mtDNA-like sequences and dynamics of infection. Parasitol Int 64:243–250. https://doi.org/10.1016/j.parint.2015.02.004
Verweyen L, Klimpel S, Palm HW (2011) Molecular phylogeny of the Acanthocephala (Class Palaeacanthocephala) with a paraphyletic assemblage of the orders Polymorphida, and Echinorhynchida. PLoS ONE 6:e28285. https://doi.org/10.1371/journal.pone.0028285
Waindok P, Lehnert K, Siebert U, Pawliczka I, Strube C (2018) Prevalence and molecular characterisation of Acanthocephala in pinnipedia of the North and Baltic Seas. Int J Parasitol Parasites Wildl 7:34–43. https://doi.org/10.1016/j.ijppaw.2018.01.002
Wang Y, Wang P, Wu D (1993) On some Echinorhynchoidea parasites from marine fishes of Fujian province, China. Wuyi Sci J 10:29–39
Weaver HJ, Smales LR (2014) Two species of Acanthocephala (Rhadinorhynchidae and Transvenidae) from elasmobranchs from Australia. Comp Parasitol 81:110–113. https://doi.org/10.1654/4654.1
Acknowledgements
We would like to acknowledge the laboratory facilities provided by Department of Zoology, Chaudhary Charan Singh University, Meerut, India. This work was supported by institutional Grants from the Department of Biology, Brigham Young University, Provo, Utah and the Institute of Parasitic Diseases, Scottsdale, Arizona, USA.
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Chaudhary, A., Amin, O.M., Heckmann, R. et al. The Molecular Phylogeny of Pararhadinorhynchus magnus Ha, Amin, Ngo, Heckmann, 2018 (Acanthocephala: Rhadinorhynchidae) from Scatophagus argus (Linn.) (Scatophagidae) in Vietnam. Acta Parasit. 65, 610–619 (2020). https://doi.org/10.2478/s11686-020-00191-5
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DOI: https://doi.org/10.2478/s11686-020-00191-5