Hostname: page-component-848d4c4894-4hhp2 Total loading time: 0 Render date: 2024-05-01T13:12:26.244Z Has data issue: false hasContentIssue false
  • English
  • Français

Echinostoma chankensis nom. nov., other Echinostoma spp. and Isthmiophora hortensis in East Asia: morphology, molecular data and phylogeny within Echinostomatidae

Published online by Cambridge University Press:  09 June 2021

Anna V. Izrailskaia Open the ORCID record for Anna V. Izrailskaia [Opens in a new window] ,
Vladimir V. Besprozvannykh  and
Yulia V. Tatonova Open the ORCID record for Yulia V. Tatonova [Opens in a new window]
Anna V. Izrailskaia*
Affiliation:
Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch, Russian Academy of Sciences, 100-letiya Street, 159, Vladivostok, 690022, Russian Federation Far Eastern Federal University, School of Biomedicine, Sukhanova, 8, Vladivostok, 690091, Russian Federation
Vladimir V. Besprozvannykh
Affiliation:
Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch, Russian Academy of Sciences, 100-letiya Street, 159, Vladivostok, 690022, Russian Federation
Yulia V. Tatonova
Affiliation:
Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch, Russian Academy of Sciences, 100-letiya Street, 159, Vladivostok, 690022, Russian Federation Far Eastern Federal University, School of Biomedicine, Sukhanova, 8, Vladivostok, 690091, Russian Federation
*
Author for correspondence: Anna V. Izrailskaia, E-mail: Anna.kharitonova92@yandex.ru
Get access Rights & Permissions [Opens in a new window]

Abstract

Life cycles, and morphological and molecular data were obtained for Echinostoma chankensis nom. nov., Echinostoma cinetorchis, Echinostoma miyagawai and Isthmiophora hortensis from East Asia. It was established that, based on both life cycle and morphology data, one of the trematodes is identical to the worms designated as Euparyphium amurensis. Genetic data showed that this trematode belongs to Echinostoma. The complex data on biological, morphological and genetic characterizations establish that the distribution of the morphologically similar species, I. hortensis and Isthmiophora melis, in the Old World are limited by the East Asian and European regions, respectively. Data on mature worms of East Asian E. miyagawai revealed morphological and genetic identity with E. miyagawai from Europe. However, E. miyagawai from Europe differs from E. miyagawai from the type locality (East Asia) in terms of reaching maturity and the morphology of cercariae. These data indicate that the European worm, designated E. miyagawai, does not belong to this species. An analysis of the phylogenetic relationships of Echinostomatidae was conducted based on the 28S, ITS2 and nad1 markers. Analysis using the nad1 gene for the known representatives of Echinostomatidae is carried out for the first time, showing that nuclear markers are ineffective separate from mitochondrial ones.

Keywords

Echinostoma chankensis nom. novEchinostomatidaelife cyclemorphological descriptionphylogenetic relationships
Type
Research Article
Information
Parasitology , Volume 148 , Issue 11 , September 2021 , pp. 1366 - 1382
Copyright
Copyright © The Author(s), 2021. 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

Ahn, YK, Ryang, YS, Chai, JY and Sohn, WM (1989) Cercarial shedding of Echinostoma cinetorchis and experimental infection of the cercariae to several kinds of snails. The Korean Journal of Parasitology 27, 203–211.CrossRefGoogle ScholarPubMed
Ando, R and Ozaki, Y (1923) On four new species of trematodes of the family Echinostomatidae. Dobutsugaku Zasshi 35, 108–119. (In Japanese).Google Scholar
Bashkirova, EY (1941) Echinostomatids of birds of the USSR and a review of their life-cycles. Writings of the Bashkir Scientific Research Veterinary Station 3, 243–300. (In Russian).Google Scholar
Beaver, PC (1941) Studies on the life history of Euparyphium melis (Trematoda: Echinostomatidae). Journal of Parasitology 27, 35–44.CrossRefGoogle Scholar
Besprozvannykh, VV (2001) Structure and life cycles of trematodes Euparyphium melis and Euparyphium amurensis sp. n (Echinostomatidae) in the Primorsky region. Russian Journal of Zoology 80, 5–11. (In Russian).Google Scholar
Besprozvannykh, VV, Ermolenko, AV and Nadtochy, EV (2012) Parasites of Animals and Humans in the South of the Far East. Part 2. Trematodes. Vladivostok, The Russian Federation: Dalnauka (In Russian).Google Scholar
Besprozvannykh, VV, Tatonova, YV and Shumenko, PG (2019) Life cycle, morphology of developmental stages of Metorchis ussuriensis sp. nov. (Trematoda: Opisthorchiidae), and phylogenetic relationships with other opisthorchiids. Journal of Zoological Systematics and Evolutionary Research 57, 24–40.CrossRefGoogle Scholar
Chung, PR, Jung, Y and Park, YK (2001 a) Segmentina hemisphaerula: a new molluscan intermediate host for Echinostoma cinetorchis in Korean. Journal of Parasitology 87, 1169–1171.CrossRefGoogle Scholar
Chung, PR, Jung, Y, Park, YK and Hwang, MK (2001 b) Austropeplea ollula (Pulmonata: Lymnaeidae): a new molluscan intermediate host of a human intestinal fluke, Echinostoma cinetorchis (Trematoda: Echinostomatidae) in Korea. Journal of Parasitology 39, 247–253.Google 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
Detwiler, JT, Bos, DH and Minchella, DJ (2010) Revealing the secret lives of cryptic species: examining the phylogenetic relationships of echinostoma parasites in North America. Molecular Phylogenetics and Evolution 55, 611–620.CrossRefGoogle ScholarPubMed
Detwiler, JT, Zajac, AM, Minchella, DJ and Belden, LK (2012) Revealing cryptic parasite diversity in a definitive host: echinostomes in muskrats. Journal of Parasitology 98, 1148–1155.CrossRefGoogle Scholar
Esteban, JG, Toledo, R, Sanchez, L and Munoz-Antol, C (1997) Life-cycle of Euparyphium albuferensis n. sp. (Trematoda: Echinostomatidae) from rats in Spain. Systematic Parasitology 38, 211–219.CrossRefGoogle Scholar
Faltynkova, A, Georgieva, S, Soldanova, M and Kostadinova, A (2015) A re-assessment of species diversity within the ‘revolutum'group of Echinostoma Rudolphi, 1809 (Digenea: Echinostomatidae) in Europe. Systematic Parasitology 90, 1–25.CrossRefGoogle ScholarPubMed
Georgieva, S, Kostadinova, A and Skirnisson, K (2012) The life-cycle of Petasiger islandicus Kostadinova, Skirnisson, 2007 (Digenea: Echinostomatidae) elucidated with the aid of molecular data. Systematic Parasitology 82, 177–183.CrossRefGoogle ScholarPubMed
Georgieva, S, Faltynkova, A, Brown, R, Blasco-Costa, I, Soldanova, M, Sitko, J, Scholz, T and Kostadinova, A (2014) Echinostoma ‘revolutum’ (Digenea: Echinostomatidae) species complex revisited: species delimitation based on novel molecular and morphological data gathered in Europe. Parasites & Vectors 7, 520.Google ScholarPubMed
Hernandez-Cruz, E, Hernandez-Orts, JS, Sereno-Uribe, AL, Perez-Ponce de Leon, G and Garcia-Varela, M (2017) Multilocus phylogenetic analysis and morphological data reveal a new species composition of the genus Drepanocephalus Dietz, 1909 (Digenea: Echinostomatidae), parasites of fish-eating birds in the Americas. Journal of Helminthology 92, 572–595.CrossRefGoogle Scholar
Hildebrand, J, Adamczyk, M, Laskowski, Z and Zalesny, G (2015) Host-dependent morphology of Isthmiophora melis (Schrank, 1788) Luhe, 1909 (Digenea, Echinostomatinae) – morphological variation vs molecular stability. Parasites & Vectors 8, 481.CrossRefGoogle ScholarPubMed
Ito, J (1964) A monograf of cercariae in Japan and adjacent territories. Progress Med Parasitolge in Japan 1, 395–550.Google Scholar
Kostadinova, A and Gibson, DI (2002) Isthmiophora Lühe, 1909 and Euparyphium Dietz, 1909 (Digenea: Echinostomatidae) re-defined, with comments on their nominal species. Systematic Parasitology 52, 205–217.CrossRefGoogle ScholarPubMed
Kostadinova, A, Gibson, DI, Biserkov, V and Ivanova, R (2000 a) A quantitative approach to the evaluation of the morphological variability of two echinostomes, Echinostoma miyagawai Ishii, 1932 and E. revolutum (Frölich, 1802) from Europe. Systematic Parasitology 45, 1–15.CrossRefGoogle Scholar
Kostadinova, A, Gibson, DI, Biserkov, V and Chipev, N (2000 b) Re-validation of Echinostoma miyagawai Ishii, 1932 (Digenea: Echinostomatidae) on the basis of the experimental completion of its life-cycle. Systematic Parasitology 45, 81–108.CrossRefGoogle ScholarPubMed
Kostadinova, A, Herniou, EA, Barrett, J and Littlewood, DT (2003) Phylogenetic relationships of Echinostoma Rudolphi, 1809 (Digenea:Echinostomatidae) and related genera re-assessed via DNA and morphological analyses. Systematic Parasitology 54, 159–176.CrossRefGoogle ScholarPubMed
Kosupko, GA (1969) The morphological peculiarities of Echinosloma revolutum and E. miyagowai cercariae. Writings of the All-Union Institute of Helminthology named after K.I. Skrjabin 15, 159–165. (ln Russian).Google Scholar
Kosupko, GA (1971) New data on the bioecology and morphology of Echinostoma revolutum and E. miyagawai (Trematoda: Echinostomatidae). Writings of the All-Union Institute of Helminthology named after K.I. Skrjabin 5, 43–49. (In Russian).Google Scholar
Lee, SH, Chai, JY, Hong, ST and Sohn, WM (1990) Experimental life history of Echinostoma cinetorchis. The Korean Journal of Parasitology 28, 39–44.CrossRefGoogle ScholarPubMed
Mohanta, UK, Watanabe, T, Anisuzzaman, OY and Itagaki, T (2019) Characterization of Echinostoma revolutum and Echinostoma robustum from ducks in Bangladesh based on morphology, nuclear ribosomal ITS2 and mitochondrial nad1 sequences. Parasitology International 69, 1–7.CrossRefGoogle ScholarPubMed
Morgan, JAT 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
Morgan, JAT and Blair, D (1998 a) Relative merits of nuclear ribosomal internal transcribed spacers and mitochondrial CO1 and ND1 genes for distinguishing among Echinostoma species (Trematoda). Parasitology 16, 289–297.CrossRefGoogle Scholar
Morgan, JAT and Blair, D (1998 b) Mitochondrial ND1 gene sequences used to identify echinostoma isolates from Australia and New Zealand. International Journal for Parasitology 28, 493–502.CrossRefGoogle ScholarPubMed
Morley, N, Adam, M and Lewis, J (2010) The effects of host size and temperature on the emergence of Echinoparyphium recurvatum cercariae from Lymnaea peregra under natural light conditions. Journal of Helminthology 84, 317–326.CrossRefGoogle ScholarPubMed
Nasincova, V (1991) The life cycle of Echinostoma bolshewense (Kotova, 1939) (Trematoda: Echinostomatidae). Folia Parasitologica 38, 143–154.Google Scholar
Nevostrueva, LS (1953) The study of the development cycle of Echinostoma miyagovai (Ishii, 1932), the causative agent of poultry echinostomiasis. Reports of the Academy of Sciences of the USSR 90, 317–318. (In Russian).Google Scholar
Nguyen, TL, Ha, ZN and Ermolenko, AV (2013) Trematodes of Terrestrial Vertebrates of Vietnam. Vladivostok, The Russian Federation: Dalnauka, (In Russian).Google Scholar
Nugaraite, D, Mazeika, V and Paulauskas, A (2017) Molecular and morphological characterization of Isthmiophora melis (Schrank, 1788) Luhe, 1909 (Digenea: Echinostomatidae) from American mink (Neovison vison) and European polecat (Mustela putorius) in Lithuania. Helminthologia 54, 97–104.CrossRefGoogle Scholar
Oshmarin, PG (1963) Parasitic Worms of Mammals and Birds in the Primorsky Region. Moscow: USSR: Academy of Science of USSR, (In Russian).Google Scholar
Radev, V, Kanev, I, Khrusanov, D and Fried, B (2009) Life cycle of Isthmiophora melis (Trematoda: Echinostomatidae) based on materials from South-Eastern Europe. Parasitology 43, 445–453. (In Russian).Google Scholar
Ronquist, F and Huelsenbeck, JP (2003) MrBayes 3, Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Sitko, J, Bizos, J, Sherrard-Smith, E, Stanton, DWG and Komorova, P (2016) Integrative taxonomy of European parasitic flatworms of the genus Metorchis Looss, 1899 (Trematoda: Opisthorchiidae). Parasitology International 65, 258–267.CrossRefGoogle Scholar
Sohn, WM, Na, BK and Shin, SS (2017) New definitive hosts and differential body indices of Isthmiophora hortensis (Digenea: echinostomatidae). The Korean Journal of Parasitology 55, 287–294.CrossRefGoogle Scholar
Staneviciute, G, Stunzenas, V and Petkeviciute, R (2015) Phylogenetic relationships of some species of the family Echinostomatidae Odner, 1910 (Trematoda), inferred from nuclear rDNA sequences and karyological analysis. Comparative Cytogenetics 9, 257–270.CrossRefGoogle Scholar
Tamura, K, Peterson, D, Peterson, N, Stecher, G, Nei, M and Kumar, S (2011) MEGA5, Molecular evolutionary genetic analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Tatonova, YV, Izrailskaia, AV and Besprozvannykh, VV (2020) Stephanoprora amurensis sp. nov., Echinochasmus milvi Yamaguti, 1939 and E. suifunensis Besprozvannykh, 1991 from the Russian southern Far East and their phylogenetic relationships within the Echinochasmidae Odhner 1910. Parasitology 147, 1469–1479.CrossRefGoogle Scholar
Tkach, VV, Kudlai, O and Kostadinova, A (2016) Molecular phylogeny and systematics of the Echinostomatoidea Looss, 1899 (Platyhelminthes: Digenea). International Journal for Parasitology 46, 171–185.CrossRefGoogle Scholar
Truett, GE, Heeger, P, Mynatt, RL, Truett, AA, Walker, JA and Warman, ML (2000) Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). BioTechniques 29, 52–54.CrossRefGoogle Scholar
Vilas, R, Criscione, CD and Blouin, MS (2005) A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology 131, 1–8.CrossRefGoogle ScholarPubMed
Winker, K, McCracken, KG, Gibson, DD, Pruett, CL, Meier, R, Huettmann, F, Wege, M, Kulikova, IV, Zhuravlev, YN, Perdue, ML, Spackman, E, Suarez, DL and Swayne, DE (2007) Movements of birds and avian influenza from Asia into Alaska. Emerging Infectious Diseases 13, 547–552.CrossRefGoogle ScholarPubMed
Yamaguti, S (1939) Studies on the helminth fauna of Japan. Part 25. Trematodes of birds, IV. Japanese Journal of Sanitary Zoology 8, 211–230.Google Scholar
Supplementary material: File

Izrailskaia et al. supplementary material

Izrailskaia et al. supplementary material

Download Izrailskaia et al. supplementary material(File)
File 4.3 MB