Hostname: page-component-848d4c4894-4hhp2 Total loading time: 0 Render date: 2024-05-15T05:53:56.948Z Has data issue: false hasContentIssue false
  • English
  • Français

Three new species of Helicometroides Yamaguti, 1934 from Japan and Australia, with new molecular evidence of a widespread species

Published online by Cambridge University Press:  26 January 2022

Nicholas Q-X. Wee Open the ORCID record for Nicholas Q-X. Wee [Opens in a new window] ,
Thomas H. Cribb Open the ORCID record for Thomas H. Cribb [Opens in a new window] ,
Sho Shirakashi Open the ORCID record for Sho Shirakashi [Opens in a new window]  and
Scott C. Cutmore Open the ORCID record for Scott C. Cutmore [Opens in a new window]
Nicholas Q-X. Wee*
Affiliation:
School of Biological Sciences, The University of Queensland, St Lucia, QLD 4072, Australia
Thomas H. Cribb
Affiliation:
School of Biological Sciences, The University of Queensland, St Lucia, QLD 4072, Australia
Sho Shirakashi
Affiliation:
Aquaculture Research Institute, Kindai University, Shirahama 3153, Nishimuro, Wakayama 649-2211, Japan
Scott C. Cutmore
Affiliation:
School of Biological Sciences, The University of Queensland, St Lucia, QLD 4072, Australia
*
Author for correspondence: Nicholas Q-X. Wee, E-mail: qi.wee@uqconnect.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

We report specimens of monorchiids infecting Haemulidae from the waters off Japan and Australia; these specimens represent five species of Helicometroides Yamaguti, 1934, three of which are unambiguously new. Helicometroides murakamii n. sp. infects Diagramma pictum pictum from off Minabe, Japan; Helicometroides gabrieli n. sp. infects Plectorhinchus chrysotaenia from off Lizard Island, Australia; and Helicometroides wardae n. sp. infects Plectorhinchus flavomaculatus and Plectorhinchus multivittatus from off Heron Island, Australia. Helicometroides murakamii n. sp. and H. gabrieli n. sp. conform to the most recent diagnosis of Helicometroides in lacking a terminal organ, but H. wardae n. sp. possesses a terminal organ with distinct, robust spines; despite this morphological distinction, the three form a strongly-supported clade in phylogenetic analyses. We also report specimens morphologically consistent with Helicometroides longicollis Yamaguti, 1934, from D. pictum pictum from off Minabe, Japan, and Diagramma pictum labiosum on the Great Barrier Reef, Australia. Genetic analyses of ITS2 rDNA, 28S rDNA and cox1 mtDNA sequence data for the Japanese specimens reveal the presence of two distinct genotypes. Specimens of the two genotypes were discovered in mixed infections and are morphologically indistinguishable; neither genotype can be associated definitively with H. longicollis as originally described. We thus identify them as H. longicollis lineage 1 and 2, pending study of further fresh material. Genetic analyses of specimens from the Great Barrier Reef are consistent with the presence of only H. longicollis lineage 1. This species thus has a range that incorporates at least Australia and Japan, localities separated by over 7000 km.

Keywords

Cryptic speciesHelicometroidesMonorchiidaesystematicstaxonomytropical Indo-west Pacific
Type
Research Article
Information
Parasitology , Volume 149 , Issue 5 , April 2022 , pp. 622 - 639
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmad, J (1982) Studies on digenetic trematodes of the families Monorchiidae and Lepocreadiidae from marine fishes of India. Kanpur University Research Journal (Science) 1, 53–69.Google Scholar
Andres, MJ, Pulis, EE, Curran, SS and Overstreet, RM (2018) On the systematics of some marine haploporids (Trematoda) with the description of a new species of Megasolena Linton, 1910. Parasitology International 67, 805–815.CrossRefGoogle ScholarPubMed
Atopkin, DM, Besprozvannykh, VV, Ngo, HD, Van Ha, N, Van Tang, N, Ermolenko, AV and Beloded, AY (2017) Morphometric and molecular data of the two digenean species Lasiotocus lizae Liu, 2002 (Monorchiidae) and Paucivitellosus vietnamensis sp. n. (Bivesiculidae) from mullet fish in Tonkin Bay, Vietnam. Journal of Helminthology 91, 346–355.CrossRefGoogle Scholar
Besprozvannykh, VV, Ermolenko, AV and Atopkin, DM (2012) The life cycle of Asymphylodora percotti sp. n. (Trematoda: Lissorchiidae) in the Russian Southern Far East. Parasitology International 61, 235–241.CrossRefGoogle Scholar
Bray, RA and Cribb, TH (2001) A review of the family Enenteridae Yamaguti, 1958 (Digenea), with descriptions of species from Australian waters, including Koseiria huxleyi n. sp. Systematic Parasitology 48, 1–29.CrossRefGoogle Scholar
Bray, RA, Cutmore, SC and Cribb, TH (2018) Lepotrema Ozaki, 1932 (Lepocreadiidae: Digenea) from Indo-Pacific fishes, with the description of eight new species, characterised by morphometric and molecular features. Systematic Parasitology 95, 693–741.CrossRefGoogle ScholarPubMed
Bray, RA, Cutmore, SC and Cribb, TH (2021) A paradigm for the recognition of cryptic trematode species in tropical Indo-west Pacific fishes: the problematic genus Preptetos (Trematoda: Lepocreadiidae). International Journal for Parasitology 52, 169–203.CrossRefGoogle Scholar
Cribb, TH and Bray, RA (2010) Gut wash, body soak, blender and heat-fixation: approaches to the effective collection, fixation and preservation of trematodes of fishes. Systematic Parasitology 76, 1–7.CrossRefGoogle Scholar
Cribb, TH, Anderson, GR, Adlard, RD and Bray, RA (1998) A DNA-based demonstration of a three-host life-cycle for the Bivesiculidae (Platyhelminthes: Digenea). International Journal for Parasitology 28, 1791–1795.CrossRefGoogle Scholar
Cribb, TH, Wee, NQ-X, Bray, RA, Cutmore, SC (2018) Monorchis lewisi n. sp. (Trematoda: Monorchiidae) from the surf bream, Acanthopagrus australis (Sparidae) in Moreton Bay, Australia. Journal of Helminthology 92, 100–108.CrossRefGoogle Scholar
Cutmore, SC, Yong, RQ-Y, Reimer, JD, Shirakashi, S, Nolan, MJ and Cribb, TH (2021) Two new species of threadlike blood flukes (Aporocotylidae), with a molecular revision of the genera Ankistromeces Nolan & Cribb, 2004 and Phthinomita Nolan & Cribb, 2006. Systematic Parasitology 98, 641–664.CrossRefGoogle ScholarPubMed
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
Diagne, PM, Quilichini, Y, Bâ, CT, Ndiaye, PI, Dione, A and Marchand, B (2015) Ultrastructure of the spermatozoon of Helicometroides atlanticus (Digenea, Monorchiidae), an intestinal parasite of Parapristipoma octolineatum (Pisces, Teleostei) in Senegal. Tissue and Cell 47, 198–204.CrossRefGoogle Scholar
Durio, WO and Manter, HW (1968) Some digenetic trematodes of marine fishes of New Caledonia. Part. 1. Bucephalidae, Monorchiidae, and some smaller families. Proceedings of the Helminthological Society of Washington 35, 143–153.Google Scholar
Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.CrossRefGoogle ScholarPubMed
Elwood, HJ, Olson, GJ and Sogin, ML (1985) The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. Molecular Biology and Evolution 2, 399–410.Google ScholarPubMed
Gaevskaya, AV and Aleshkina, LD (1983) [New data on the trematodes from fishes of Atlantic coast of Africa]. Parazitologiia 17, 12–17. [In Russian].Google Scholar
Gibson, DI and Bray, RA (1982) A study and reorganization of Plagioporus Stafford, 1904 (Digenea: Opecoelidae) and related genera, with special reference to forms from European Atlantic waters. Journal of Natural History 16, 529–559.CrossRefGoogle Scholar
Huston, DC, Cutmore, SC, Miller, TL, Sasal, P, Smit, NJ and Cribb, TH (2021) Gorgocephalidae (Digenea: Lepocreadioidea) in the Indo-West Pacific: new species, life-cycle data and perspectives on species delineation over geographic range. Zoological Journal of the Linnean Society 193, 1416–1455.CrossRefGoogle Scholar
ICZN (2012) International Commission on Zoological Nomenclature: amendment of articles 8, 9, 10, 21 and 78 of the International Code of Zoological Nomenclature to expand and refine methods of publication. Bulletin of Zoological Nomenclature 69, 161–169.CrossRefGoogle Scholar
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Mentjies, P and Drummond, A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.CrossRefGoogle ScholarPubMed
Littlewood, DTJ and Olson, PD (2001) Small subunit rDNA and the Platyhelminthes: signal, noise, conflict and compromise. In Littlewood, DTJ and Bray, RA (eds), Interrelationships of the Platyhelminthes. London: Taylor and Francis, pp. 262–278.Google Scholar
Littlewood, DTJ, Rohde, K and Clough, KA (1997) Parasite speciation within or between host species? Phylogenetic evidence from site-specific polystome monogeneans. Parasitology 27, 1289–1297.Google ScholarPubMed
Littlewood, DTJ, Curini-Galletti, M and Herniou, EA (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution 16, 449–466.CrossRefGoogle ScholarPubMed
Lockyer, A, Olson, PD and Littlewood, DTJ (2003) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biological Journal of the Linnean Society 78, 155–171.CrossRefGoogle Scholar
Maddison, WP and Maddison, DR (2019) Mesquite: a modular system for evolutionary analysis. Version 3.6.Google Scholar
Madhavi, R (1974) Digenetic trematodes from marine fishes of Waltair Coast, Bay of Bengal. Family Monorchiidae. Rivista di Parassitologia 35, 87–98.Google Scholar
Madhavi, R (2008) Family Monorchiidae Odhner, 1911. In Bray, RA, Gibson, DI and Jones, A (eds), Keys to the Trematoda, Volume 3. Wallingford-London: CAB International and Natural History Museum, pp. 145–175.Google Scholar
Martin, SB, Cutmore, SC and Cribb, TH (2017) Revision of Neolebouria Gibson, 1976 (Digenea: Opecoelidae), with Trilobovarium n. g., for species infecting tropical and subtropical shallow-water fishes. Systematic Parasitology 94, 307–338.CrossRefGoogle Scholar
McNamara, MKA and Cribb, TH (2011) Taxonomy, host specificity and dietary implications of Hurleytrematoides (Digenea: Monorchiidae) from chaetodontid fishes on the Great Barrier Reef. Parasitology International 60, 255–269.CrossRefGoogle ScholarPubMed
McNamara, MKA, Miller, TL and Cribb, TH (2014) Evidence for extensive cryptic speciation in trematodes of butterflyfishes (Chaetodontidae) of the tropical Indo-West Pacific. International Journal for Parasitology 44, 37–48.CrossRefGoogle ScholarPubMed
Miller, MA, Pfeiler, E and Schwartz, T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE). New Orleans, LA, pp. 1–8.CrossRefGoogle Scholar
Morgan, JA and Blair, D (1995) Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: an aid to establishing relationships within the 37-collar-spine group. Parasitology 111, 609–615.CrossRefGoogle ScholarPubMed
Olson, PD, Cribb, TH, Tkach, VV, Bray, RA and Littlewood, DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733–755.CrossRefGoogle Scholar
Panyi, AJ, Curran, SS and Overstreet, RM (2020) Phylogenetic affinity of Genolopa (Digenea: Monorchiidae) with descriptions of two new species. Diversity 12, 51.CrossRefGoogle Scholar
Pleijel, F, Jondelius, U, Norlinder, E, Nygren, A, Oxelman, B, Schander, C, Sundberg, P and Thollesson, M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution 48, 369–371.CrossRefGoogle Scholar
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DI, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Sambrook, J and Russell, DW (2001) Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press.Google Scholar
Searle, EL, Cutmore, SC and Cribb, TH (2014) Monorchiid trematodes of the painted sweetlips, Diagramma labiosum (Perciformes: Haemulidae), from the southern Great Barrier Reef, including a new genus and three new species. Systematic Parasitology 88, 195–211.CrossRefGoogle Scholar
Snyder, SD and Tkach, VV (2001) Phylogenetic and biogeographical relationships among some Holarctic frog lung flukes (Digenea: Haematoloechidae). Journal of Parasitology 87, 1433–1440.CrossRefGoogle Scholar
Sokolov, SG and Gordeev, II (2019) Asaccotrema vietnamiense n. gen.; n. sp. (Trematoa: Monorchioidea), a new aberrant representative of lissorchiid trematodes from the sidestripe rasbora, Rasbora paviana Tirant (Actinopterygii: Cyprinidae), Vietnam. Zootaxa 4674, 451–462.CrossRefGoogle Scholar
Sokolov, SG, Voropaeva, E and Atopkin, DM (2020) A new species of deropristid trematode from the sterlet Acipenser ruthenus (Actinopterygii: Acipenseridae) and revision of superfamily affiliation of the family Deropristidae. Zoological Journal of the Linnean Society 190, 448–459.CrossRefGoogle Scholar
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.CrossRefGoogle ScholarPubMed
Swofford, DL (2002) PAUP*. Phylogenetic Analyses Using Parsimony (*and other methods). Version 4.0b10. Sinauer Associates, Sunderland, Massachusetts.Google Scholar
Tkach, VV, Pawlowski, J, Mariauxc, J and Swiderski, Z (2001) Molecular phylogeny of the suborder Plagiorchiata and its position in the system of Digenea. In Littlewood, D and Bray, RA (eds), Interrelationships of Platyhelminthes. London: Taylor and Francis, pp. 186–193.Google Scholar
Wee, NQ-X, Cribb, TH, Bray, RA and Cutmore, SC (2017 a) Two known and one new species of Proctoeces from Australian teleosts: variable host-specificity for closely related species identified through multi-locus molecular data. Parasitology International 66, 16–26.CrossRefGoogle ScholarPubMed
Wee, NQ-X, Cutmore, SC, Yong, RQ-Y and Cribb, TH (2017 b) Two new and one known species of Tergestia Stossich, 1899 (Trematoda: Fellodistomidae) with novel molecular characterisation for the genus. Systematic Parasitology 94, 861–874.CrossRefGoogle ScholarPubMed
Wee, NQ-X, Cutmore, SC and Cribb, TH (2018) Two monorchiid species from the freckled goatfish, Upeneus tragula (Perciformes: Mullidae), in Moreton Bay, Australia, including a proposal of a new genus. Systematic Parasitology 95, 353–365.CrossRefGoogle Scholar
Wee, NQ-X, Cutmore, SC and Cribb, TH (2019) Four new monorchiids from the golden trevally, Gnathanodon speciosus (Forsskål) (Perciformes: Carangidae), in Moreton Bay, Australia. Systematic Parasitology 96, 265–278.CrossRefGoogle Scholar
Wee, NQ-X, Cribb, TH, Cutmore, SC and Martin, SB (2020 a) Retroporomonorchis pansho n. gen. n. sp., an unusual monorchiid trematode exploiting an atypical host. Systematic Parasitology 97, 441–454.CrossRefGoogle Scholar
Wee, NQ-X, Crouch, K, Cutmore, SC and Cribb, TH (2020 b) Pseudohurleytrema yolandae n. sp., the first monorchiid trematode reported from the Triacanthidae (Tetraodontiformes). Systematic Parasitology 97, 491–500.CrossRefGoogle Scholar
Wee, NQ-X, Cutmore, SC, Pérez-del-Olmo, A and Cribb, TH (2020 c) First steps to restructuring the problematic genus Lasiotocus Looss, 1907 (Digenea: Monorchiidae) with the proposal of four new genera. Parasitology International 79. doi: https://doi.org/10.1016/j.parint.2020.102164CrossRefGoogle ScholarPubMed
Wee, NQ-X, Cutmore, SC, Sasal, P and Cribb, TH (2020 d) Three new species of Allobacciger Hafeezullah & Siddiqi, 1970 (Digenea: Monorchiidae) from Australia and French Polynesia. Marine Biodiversity 50. doi: https://doi.org/10.1007/s12526-019-01029-8sCrossRefGoogle Scholar
Wee, NQ-X, Cribb, TH, Corner, RD, Ward, S and Cutmore, SC (2021 a) Gastropod first intermediate hosts for two species of Monorchiidae Odhner, 1911 (Trematoda): I can't believe it's not bivalves!. International Journal for Parasitology 51, 1035–1046.CrossRefGoogle Scholar
Wee, NQ-X, Cutmore, SC and Cribb, TH (2021 b) Gerricola queenslandensis n. g., n. sp., a new monorchiid trematode from the eastern Australian coast, with details on its asexual stages. Journal of Helminthology 95. doi: https://doi.org/10.1017/s0022149x21000213CrossRefGoogle Scholar
Xia, X (2018) DAMBE7: new and improved tools for data analysis in molecular biology and evolution. Molecular Biology and Evolution 35, 1550–1552.CrossRefGoogle ScholarPubMed
Xia, X and Lemey, P (2009) Assessing substitution saturation with DAMBE. In Lemey, P, Salemi, M and Vandamme, A-M (eds), The Phylogenetic Handbook: A Practical Approach to DNA and Protein Phylogeny. Cambridge: University Press, pp. 615–630.CrossRefGoogle Scholar
Xia, X, Xie, Z, Salemi, M, Chen, L and Wang, Y (2003) An index of substitution saturation and its application. Molecular Phylogenetics and Evolution 26, 1–7.CrossRefGoogle ScholarPubMed
Yamaguti, S (1934) Studies on the helminth fauna of Japan. Part II. Trematodes of fishes, I. Japanese Journal of Zoology 5, 249–541.Google Scholar
Yamaguti, S (1971) Synopsis of Digenetic Trematodes of Vertebrates Vol. 1. Tokyo: Keigaku Publishing.Google Scholar