Advertisement

Parasitology Research

, Volume 118, Issue 12, pp 3253–3265 | Cite as

A new species of Clinostomum Leidy, 1856 in East Asia based on genomic and morphological data

  • Sean A. LockeEmail author
  • Monica Caffara
  • Daniel Barčák
  • Pasaikou Sonko
  • Perla Tedesco
  • Maria L. Fioravanti
  • Wenxiang Li
Fish Parasitology - Original Paper

Abstract

Metacercariae of Clinostomum Leidy, 1856 are frequently encountered in freshwater fish. In 2015, a provisional species of Clinostomum in People’s Republic of China (PRC) was distinguished from C. complanatum (Rudolphi, 1819) in Europe based on divergent cytochrome c oxidase I (CO1). However, in subsequent studies in East Asia, the same divergent CO1 genotype was identified as C. complanatum. These matching sequences suggest that either the provisional East Asian species was incorrectly distinguished from C. complanatum in 2015 or that C. complanatum in East Asia was misidentified in later studies. We tested these alternatives by sequencing the mitochondrial genome of C. complanatum in Italy, which was 5.7% divergent from a previously published sequence from Clinostomum in PRC, including differences in 80 of 3390 (2.4%) translated amino acids. Partial CO1 sequences of specimens from PRC and those from Italy, Romania, and Turkey also each formed reciprocally monophyletic clades. Partial CO1 from the East Asian clade varied by mean 3.6% (range 2.4–4.8%) from C. complanatum from Italy, Romania, and Turkey; mean intra-clade CO1 variation was 0.3% (range 0–1.9%). Metacercariae from Europe and East Asia display significant morphometric variation, and data from the literature suggest morphological differences in the genital complex of adults. Although sequences of nuclear rDNA did not differ between isolates from the west and East Asia, taken together, these results lead us to describe a new species of Clinostomum.

Keywords

Yellow grub Halzoun Helminth Fish parasite Molecular prospecting DNA barcode Species identification 

Notes

Funding information

This work was supported by grants from the Puerto Rico Science, Technology and Research Trust (2016-00080) (SL), the National Science Foundation (1845021) (SL), and the Joint Research Project of the Slovak Academy of Sciences and Taiwan Ministry of Science and Technology (SAS-MOST JRP 2016/7, MOST 106-2923-B-038-001-MY3) (DB).

Compliance with ethical standards

All applicable international, national, and institutional guidelines for the care and use of animals were followed (MNSDG000000034589 issued by Rezervaţia Biosferei Delta Dunării in Tulcea, Romania).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

436_2019_6536_MOESM1_ESM.xlsx (13 kb)
ESM 1 Measurements of metacercariae of Clinostomum (in μm) from the present and other studies, given as range (mean ± standard deviation, n measured). (XLSX 13 kb)
436_2019_6536_MOESM2_ESM.fasta (20 kb)
ESM 2 Alignment of partial sequences of cytochrome c oxidase I used for phylogenetic analysis (see Fig. 3). (FASTA 20 kb)

References

  1. Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, Pütz J, Middendorf M, Stadler PF (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol 69:313–319.  https://doi.org/10.1016/j.ympev.2012.08.023 CrossRefPubMedGoogle Scholar
  2. Brabec J, Kostadinova A, Scholz T, Littlewood DTJ (2015) Complete mitochondrial genomes and nuclear ribosomal RNA operons of two species of Diplostomum (Platyhelminthes: Trematoda): a molecular resource for taxonomy and molecular epidemiology of important fish pathogens. Parasit Vectors 8:1–11.  https://doi.org/10.1186/s13071-015-0949-4 CrossRefGoogle Scholar
  3. Braun M (1901) Die arten der gattung Clinostomum Leidy. Zoologische Jahrbücher Abteilung für Systematik, Geographie und Biologie der Tiere 14:1–48Google Scholar
  4. Caffara M, Locke SA, Gustinelli A, Marcogliese DJ, Fioravanti ML (2011) Morphological and molecular differentiation of Clinostomum complanatum and Clinostomum marginatum (Digenea: Clinostomidae) metacercariae and adults. J Parasitol 97:884–891.  https://doi.org/10.1645/GE-2781.1 CrossRefPubMedGoogle Scholar
  5. Caffara M, Bruni G, Paoletti C, Gustinelli A, Fioravanti ML (2014) Metacercariae of Clinostomum complanatum (Trematoda: Digenea) in European newts Triturus carnifex and Lissotriton vulgaris (Caudata: Salamandridae). J Helminthol 88:278–285.  https://doi.org/10.1017/S0022149X13000151 CrossRefPubMedGoogle Scholar
  6. Caffara M, Locke SA, Cristanini C, Davidovich N, Markovich MP, Fioravanti ML (2016) A combined morphometric and molecular approach to identifying metacercariae of Euclinostomum heterostomum (Digenea: Clinostomidae). J Parasitol 102:239–248.  https://doi.org/10.1645/15-823 CrossRefPubMedGoogle Scholar
  7. Chen L, Feng Y, Chen H-M, Wang LX, Feng HL, Yang X, Mughal MN, Fang R (2016) Complete mitochondrial genome analysis of Clinostomum complanatum and its comparison with selected digeneans. Parasitol Res 115:3249–3256.  https://doi.org/10.1007/s00436-016-5102-6 CrossRefPubMedGoogle Scholar
  8. Dzikowski R, Levy M, Poore M et al (2004) Clinostomum complanatum and Clinostomum marginatum (Rudolphi, 1819) (Digenea: Clinostomidae) are separate species based on differences in ribosomal DNA. J Parasitol 90:413–414.  https://doi.org/10.1645/GE-159R CrossRefPubMedGoogle Scholar
  9. Gaglio G, Reina V, Caffara M, Gjurcevic E, Iaria C, Marino F (2016) Risk of introduction of Clinostomum complanatum (Digenea: Clinostomidae) to Sicily through use of Cobitis bilineata (Canestrini, 1865) as live baits. Bull Eur Assoc Fish Pathol 36:105–110Google Scholar
  10. Gu J, Zhuang G, Wang X, Wang Y (2015) The epidemiology and prevention of Clinostomum complanatum. Sci Fish Farm:88–88Google Scholar
  11. Gustinelli A, Caffara M, Florio D, Otachi EO, Wathuta EM, Fioravanti ML (2010) First description of the adult stage of Clinostomum cutaneum Paperna, 1964 (Digenea: Clinostomidae) from grey herons Ardea cinerea L. and a redescription of the metacercaria from the Nile tilapia Oreochromis niloticus niloticus (L.) in Kenya. Syst Parasitol 76:39–51.  https://doi.org/10.1007/s11230-010-9231-5 CrossRefPubMedGoogle Scholar
  12. Hays WL (1994) Statistics, Fifth Edition. Harcourt Brace College Publishers, Fort WorthGoogle Scholar
  13. Iwaki T, Waki T, Arakawa J, Ogawa K (2018) The Digenean Clinostomum complanatum found from Great Cormorant Phalacrocorax carbo in Japan. Fish Pathol 53:132–135.  https://doi.org/10.3147/jsfp.53.132 CrossRefGoogle Scholar
  14. Jeon H-K, Kim K-H, Eom KS (2007) Complete sequence of the mitochondrial genome of Taenia saginata: comparison with T. solium and T. asiatica. Parasitol Int 56:243–246.  https://doi.org/10.1016/j.parint.2007.04.001 CrossRefPubMedGoogle Scholar
  15. Kagei N, Yanohara Y, Uchikawa R, Sato A (1988) Natural infection with Clinostomum complanatum (Rud., 1819) in the birds of southern Japan. Jpn J Parasitol 37:254–257Google Scholar
  16. Kim Y-G, Nagasawa K (1996) Infection of Clinostomum complanatum (Rudolphi, 1814) (Trematoda: Digenea) metacercaria in goldfish (Carassius auratus) cultured in Korea. J Fish Pathol 9:1–19Google Scholar
  17. Li BF, Liu X-H, Ge H-L et al (2018) The discovery of Clinostomum complanatum metacercariae in farmed Chinese sucker, Myxocyprinus asiaticus. Aquaculture 495:273–280.  https://doi.org/10.1016/j.aquaculture.2018.05.052 CrossRefGoogle Scholar
  18. Liao X-H (1992) The biology of Clinostomum complanatum (Rud.) I. Life history. Wuyi Sci J 9:99–133Google Scholar
  19. Liu G-H, Gasser RB, Young ND, Song HQ, Ai L, Zhu XQ (2014) Complete mitochondrial genomes of the ‘intermediate form’ of Fasciola and Fasciola gigantica, and their comparison with F. hepatica. Parasit Vectors 7:150.  https://doi.org/10.1186/1756-3305-7-150 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Locke SA, Caffara M, Marcogliese DJ, Fioravanti ML (2015a) A large-scale molecular survey of Clinostomum (Digenea, Clinostomidae). Zool Scr 44:203–217.  https://doi.org/10.1111/zsc.12096 CrossRefGoogle Scholar
  21. Locke SA, Al-Nasiri FS, Caffara M et al (2015b) Diversity, specificity and speciation in larval Diplostomidae (Platyhelminthes: Digenea) in the eyes of freshwater fish, as revealed by DNA barcodes. Int J Parasitol 45:841–855.  https://doi.org/10.1016/j.ijpara.2015.07.001 CrossRefPubMedGoogle Scholar
  22. Locke SA, Van Dam A, Caffara M et al (2018) Validity of the Diplostomoidea and Diplostomida (Digenea, Platyhelminthes) upheld in phylogenomic analysis. Int J Parasitol 48:1043–1059.  https://doi.org/10.1016/j.ijpara.2018.07.001 CrossRefPubMedGoogle Scholar
  23. Ma J, He J-J, Liu G-H et al (2016a) Mitochondrial genome of Ogmocotyle sikae and implications for phylogenetic studies of the Notocotylidae trematodes. Infect Genet Evol 37:208–214.  https://doi.org/10.1016/j.meegid.2015.11.018 CrossRefPubMedGoogle Scholar
  24. Ma J, He J-J, Liu G-H, Leontovyč R, Kašný M, Zhu XQ (2016b) Complete mitochondrial genome of the giant liver fluke Fascioloides magna (Digenea: Fasciolidae) and its comparison with selected trematodes. Parasit Vectors 9:429–427.  https://doi.org/10.1186/s13071-016-1699-7 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Matthews D, Cribb TH (1998) Digenetic trematodes of the genus Clinostomum Leidy, 1856 (Digenea: Clinostomidae) from birds of Queensland, Australia, including C. wilsoni n. sp. from Egretta intermedia. Syst Parasitol 39:199–208.  https://doi.org/10.1023/A:1005982530560 CrossRefGoogle Scholar
  26. Morin PA, Archer FI, Foote AD, Vilstrup J, Allen EE, Wade P, Durban J, Parsons K, Pitman R, Li L, Bouffard P, Abel Nielsen SC, Rasmussen M, Willerslev E, Gilbert MT, Harkins T (2010) Complete mitochondrial genome phylogeographic analysis of killer whales (Orcinus orca) indicates multiple species. Genome Res 20:908–916.  https://doi.org/10.1101/gr.102954.109 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Moszczynska A, Locke SA, McLaughlin JD, Marcogliese DJ, Crease TJ (2009) Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes illustrates the challenge of barcoding parasitic helminths. Mol Ecol Resour 9:75–82.  https://doi.org/10.1111/j.1755-0998.2009.02634.x CrossRefPubMedGoogle Scholar
  28. Nakao M, McManus DP, Schantz PM, Craig PS, Ito A (2007) A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134:713–722.  https://doi.org/10.1017/S0031182006001934 CrossRefPubMedGoogle Scholar
  29. Nielsen MK, Wang J, Davis R, Bellaw JL, Lyons ET, Lear TL, Goday C (2014) Parascaris univalens - a victim of large-scale misidentification? Parasitol Res 113:4485–4490.  https://doi.org/10.1007/s00436-014-4135-y CrossRefPubMedGoogle Scholar
  30. Pleijel F, Jondelius U, Norlinder E, Nygren A, Oxelman B, Schander C, Sundberg P, Thollesson M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Mol Phyl Evol 48:369-371 https://doi.org/10.1016/j.ympev.2008.03.024 CrossRefGoogle Scholar
  31. Pritchard MH, Kruse G (1982) The collection and preservation of animal parasites. University of Nebraska Press, LincolnGoogle Scholar
  32. 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. Syst Biol 61:539–542.  https://doi.org/10.1093/sysbio/sys029 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Rosser TG, Baumgartner WA, Alberson NR, Noto TW, Woodyard ET, Tommy King D, Wise DJ, Griffin MJ (2018) Clinostomum poteae n. sp. (Digenea: Clinostomidae), in the trachea of a double-crested cormorant Phalacrocorax auritus Lesson, 1831 and molecular data linking the life-cycle stages of Clinostomum album Rosser, Alberson, Woodyard, Cunningham, Pote & Griffin, 2017 in Mississippi, USA. Syst Parasitol 95:543–566.  https://doi.org/10.1007/s11230-018-9801-5 CrossRefPubMedGoogle Scholar
  34. Rudolphi C (1819) Entozoorum synopsis cui accedunt mantissa duplex et indices locupletissimi. August Rücker, BerlinCrossRefGoogle Scholar
  35. Shini KK, Preethakumari VM, Ramitha UC, Vasandakumar MV (2015) Helminth parasitic fauna of a cyprinid fish Devario malabaricus (Jerdon). Int J Fish Aquat Stud 2:175–179Google Scholar
  36. Simsek E, Yildirim A, Yilmaz E, Inci A, Duzlu O, Onder Z, Ciloglu A, Yetismis G, Pekmezci GZ (2018) Occurrence and molecular characterization of Clinostomum complanatum (Trematoda: Clinostomidae) in freshwater fishes caught from Turkey. Parasitol Res 117:2117–2124.  https://doi.org/10.1007/s00436-018-5898-3 CrossRefPubMedGoogle Scholar
  37. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313.  https://doi.org/10.1093/bioinformatics/btu033 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Ukoli F (1966) On the life history, growth and development from the metacercarial stage to adulthood, of Clinostomum tilapiae Ukoli, 1966. J Helminthol 40:215–226CrossRefGoogle Scholar
  39. Vilas R, Criscione C, Blouin M (2005) A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology 131:839–846.  https://doi.org/10.1017/S0031182005008437 CrossRefPubMedGoogle Scholar
  40. Wang M-L, Chen H-Y, Shih H-H (2017) Occurrence and distribution of yellow grub trematodes (Clinostomum complanatum) infection in Taiwan. Parasitol Res 116:1761–1771.  https://doi.org/10.1007/s00436-017-5457-3 CrossRefPubMedGoogle Scholar
  41. Woodyard ET, Rosser TG, Rush SA (2017) Alligator wrestling: morphological, molecular, and phylogenetic data on Odhneriotrema incommodum (Leidy, 1856) (Digenea: Clinostomidae) from Alligator mississippiensis Daudin, 1801 in Mississippi, USA. Parasitol Res 116:2981–2993.  https://doi.org/10.1007/s00436-017-5607-7 CrossRefPubMedGoogle Scholar
  42. Wu S (2015) Aquatic animal parasites. China Agriculture Press, BeijingGoogle Scholar
  43. Zhou G, Xiang S-L, Shi L (2008) The occurrence and control of the disease caused by Clinostomum complanatum. Fish Sci Technol Inf 35:301-303Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Sean A. Locke
    • 1
    Email author
  • Monica Caffara
    • 2
  • Daniel Barčák
    • 3
  • Pasaikou Sonko
    • 4
    • 5
  • Perla Tedesco
    • 2
  • Maria L. Fioravanti
    • 2
  • Wenxiang Li
    • 6
  1. 1.Department of BiologyUniversity of Puerto Rico at MayagüezMayagüezPuerto Rico
  2. 2.Department of Veterinary Medical SciencesAlma Mater Studiorum University of BolognaOzzano EmiliaItaly
  3. 3.Institute of Parasitology, SASKošiceSlovak Republic
  4. 4.Department of International PhD Program in Medicine, College of MedicineTaipei Medical UniversityTaipeiTaiwan
  5. 5.Department of Molecular Parasitology and Tropical Diseases, School of Medicine, College of MedicineTaipei Medical UniversityTaipeiTaiwan
  6. 6.Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of HydrobiologyChinese Academy of SciencesWuhanPeople’s Republic of China

Personalised recommendations