Hostname: page-component-848d4c4894-2xdlg Total loading time: 0 Render date: 2024-07-01T19:12:47.618Z Has data issue: false hasContentIssue false
  • English
  • Français

A new species of Echinostoma (Trematoda: Echinostomatidae) from the ‘revolutum’ group found in Brazil: refuting the occurrence of Echinostoma miyagawai (=E. robustum) in the Americas

Published online by Cambridge University Press:  28 October 2021

Marisa C. Valadão ,
Danimar López-Hernández ,
Philippe V. Alves  and
Hudson A. Pinto Open the ORCID record for Hudson A. Pinto [Opens in a new window]
Marisa C. Valadão
Affiliation:
Department of Parasitology, Laboratório de Biologia de Trematoda, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, P.O. Box 486, 30123-970, Belo Horizonte, Minas Gerais, Brazil.
Danimar López-Hernández
Affiliation:
Department of Parasitology, Laboratório de Biologia de Trematoda, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, P.O. Box 486, 30123-970, Belo Horizonte, Minas Gerais, Brazil.
Philippe V. Alves*
Affiliation:
Department of Parasitology, Laboratório de Biologia de Trematoda, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, P.O. Box 486, 30123-970, Belo Horizonte, Minas Gerais, Brazil.
Hudson A. Pinto
Affiliation:
Department of Parasitology, Laboratório de Biologia de Trematoda, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, P.O. Box 486, 30123-970, Belo Horizonte, Minas Gerais, Brazil.
*
Author for correspondence: Hudson A. Pinto, E-mail: hudsonalves13@icb.ufmg.br
Get access Rights & Permissions [Opens in a new window]

Abstract

Although Echinostoma robustum (currently a synonym of E. miyagawai) was reported in the Americas based on molecular data, morphological support on adult parasites is still required. Herein, a new species of Echinostoma is described based on worms found in a chicken from Brazil. Molecular phylogenetic analyses based on 28S (1063 bp), ITS (947 bp) and Nad-1 (442 bp) datasets reveal the inclusion of the new species within Echinostoma ‘revolutum’ species complex. Moreover, it was verified the conspecificity between cercariae previously identified as E. robustum in Brazil [identical ITS and only 0.3% of divergence (1 nucleotide) in Nad-1]. Species discovery analyses show that these two isolates form an independent lineage (species) among Echinostoma spp. Compared to E. miyagawai, the new species presents relatively high divergence in Nad-1 (7.88–9.09%). Morphologically, the specimens are distinguished from all nominal species from the ‘revolutum’ species complex by the more posterior position of the testes (length of post-testicular field as a proportion of body length about 20%). They further differ from E. miyagawai and South American Echinostoma spp. by the higher proportion of forebody to the body length. Therefore, combined molecular and morphological evidence supports the proposal of the species named here as Echinostoma pseudorobustum sp. nov.

Keywords

EchinostomesGallus domesticusintegrative taxonomytrematodes
Type
Research Article
Information
Parasitology , Volume 149 , Issue 3 , March 2022 , pp. 325 - 336
Check for updates
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

Ailán-Choke, LG, Tavares, LER, Luque, JL and Pereira, FB (2020) An integrative approach assesses the intraspecific variations of Procamallanus (Spirocamallanus) inopinatus, a common parasite in Neotropical freshwater fishes, and the phylogenetic patterns of Camallanidae. Parasitology 147, 1752–1764.CrossRefGoogle ScholarPubMed
Altschul, SF, Gish, W, Miller, W, Myers, EW and Lipman, DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.CrossRefGoogle ScholarPubMed
Alves, PV, de Chambrier, A, Luque, JL and Scholz, T (2021) Integrative taxonomy reveals hidden cestode diversity in Pimelodus catfishes in the Neotropics. Zoologica Scripta 50, 210–224.CrossRefGoogle Scholar
Beaver, PC (1937) Experimental studies on Echinostoma revolutum (Frölich) a fluke from birds and mammals. Illinois Biological Monographs 15, 96 pp.Google Scholar
Blair, C and Bryson, RW Jr (2017) Cryptic diversity and discordance in single-locus species delimitation methods within horned lizards (Phrynosomatidae: Phrynosoma). Molecular Ecology Resources 17, 1168–1182.CrossRefGoogle Scholar
Carstens, BC, Pelletier, TA, Reid, NM and Satler, JD (2013) How to fail at species delimitation. Molecular Ecology 22, 4369–4383.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
Chai, JY, Jung, BK, Chang, T, Shin, H, Cho, J, Ryu, JY, Kim, HS, Park, K, Jeong, MH, Hoang, EH and Abullah, MBM (2021) Echinostoma miyagawai Ishii, 1932 (Echinostomatidae) from ducks in Aceh Province, Indonesia with special reference to its synonym with Echinostoma robustum Yamaguti, 1935. Korean Journal of Parasitology 59, 35–45.CrossRefGoogle Scholar
da Cruz, MOR and Weksler, M (2018) Impact of tree priors in species delimitation and phylogenetics of the genus Oligoryzomys (Rodentia: Cricetidae). Molecular Phylogenetics and Evolution 119, 1–12.CrossRefGoogle Scholar
Dellicour, S and Flot, JF (2018) The hitchhiker's guide to single-locus species delimitation. Molecular Ecology Resources 18, 1234–1246.CrossRefGoogle ScholarPubMed
Detwiler, JT, Bos, DH and Minchella, DJ (2010) Revealing the secret lives of cryptic species: examining the phylogenetic relationships of echinostome 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
Dietz, E (1910) Die Echinostomiden der Vögel. Zoologische Jahrbücher 12, 265–512.Google Scholar
Esteban, JG and Muñoz-Antoli, C (2009) Echinostomes: systematics and life cycles. In Fried, B and Toledo, R (eds), The Biology of Echinostomes: From the Molecule to the Community. New York, USA: Springer Science + Business Media, pp. 1–34.Google Scholar
Faltýnková, A, Georgieva, S, Soldánová, 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
Fried, B and Graczyk, TK (2004) Recent advances in the biology of Echinostoma species in the ‘revolutum’ group. Advances in Parasitology 58, 139–195.CrossRefGoogle ScholarPubMed
Fried, B and Huffman, JE (1996) The biology of the intestinal trematode Echinostoma caproni. Advances in Parasitology 38, 311–368.CrossRefGoogle ScholarPubMed
Fu, YT, Jin, YC, Li, F and Liu, GH (2019) Characterization of the complete mitochondrial genome of the echinostome Echinostoma miyagawai and phylogenetic implications. Parasitology Research 118, 3091–3097.CrossRefGoogle ScholarPubMed
Georgieva, S, Selbach, C, Faltýnková, A, Soldánová, M, Sures, B, Skirnisson, K and Kostadinova, A (2013) New cryptic species of the ‘revolutum’ group of Echinostoma (Digenea: Echinostomatidae) revealed by molecular and morphological data. Parasites & Vectors 6, 64.CrossRefGoogle ScholarPubMed
Georgieva, S, Faltýnková, A, Brown, R, Blasco-Costa, I, Soldánová, 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
Georgieva, S, Blasco-Costa, I and Kostadinova, A (2017) Molecular characterization of four echinostomes (Digenea: Echinostomatidae) from birds in New Zealand, with descriptions of Echinostoma novaezealandense n. sp. and Echinoparyphium poulini n. sp. Systematic Parasitology 94, 477–497.CrossRefGoogle Scholar
Heneberg, P (2020) Taxonomic comments on the validity of Echinostoma miyagawai Ischii, 1932 (Trematoda: Echinostomatidae). Parasitology International 74, 101931.CrossRefGoogle Scholar
Hsu, KC, Lie, KJ and Basch, PF (1968) The life history of Echinostoma rodriguesi sp. n. (Trematoda: Echinostomatidae). Journal of Parasitology 54, 333–339.CrossRefGoogle Scholar
Ishii, N (1932) Studies on bird trematodes. I. Jikken Igaku Zasshi 16, 1205–1231.Google Scholar
Izrailskaia, AV, Besprozvannykh, VV and Tatonova, YV (2021) Echinostoma chankensis nom. nov., other Echinostoma spp. and Isthmiophora hortensis in East Asia: morphology, molecular data and phylogeny within Echinostomatidae. Parasitology 148, 1366–1382.CrossRefGoogle ScholarPubMed
Jeyarasasingam, U, Heyneman, D, Lim, H-K and Mansoul, N (1972) Life cycle of a new echinostome from Egypt, Echinostoma liei sp. nov. (Trematoda: Echinostomatidae). Parasitology 65, 203–222.CrossRefGoogle Scholar
Kanev, I (1994) Life cycle, delimitation and redescription of Echinostoma revolutum (Froelich, 1802) (Trematoda: Echinostomatidae). Systematic Parasitology 28, 125–144.CrossRefGoogle Scholar
Kapli, P, Lutteropp, S, Zhang, J, Kobert, K, Pavlidis, P, Stamatakis, A and Flouri, T (2017) Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics 33, 1630–1638.Google ScholarPubMed
Komma, MD (1972) Revalidação da espécie Echinostoma erraticum, (Lutz, 1924). Revista de Patologia Tropical 1, 463–471.Google Scholar
Kostadinova, A (2005) Family Echinostomatidae Looss, 1899. In Jones, A, Gibson, DI and Bray, R (eds), Keys to the Trematoda. Volume 2. London, UK: CABI Publishing and The Natural History Museum, pp. 9–64.CrossRefGoogle Scholar
Kostadinova, A and Gibson, DI (2000) The systematics of the echinostomes. In Fried, B and Graczyk, TK (eds), Echinostomes as Experimental Models for Biological Research. Dordrecht: Kluwer, pp. 31–57.CrossRefGoogle Scholar
Kostadinova, A, Gibson, DI, Biserkov, V and Chipev, N (2000) 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, Barret, J and Littlewood, DTJ (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
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
Le, TH, Pham, LTK, Doan, HTT, Le, XTK, Saijuntha, W, Rajapakse, RJ and Lawton, SP (2020) Comparative mitogenomics of the zoonotic parasite Echinostoma revolutum resolves taxonomic relationships within the ‘E. revolutum’ species group and the Echinostomata (Platyhelminthes: Digenea). Parasitology 147, 566–576.CrossRefGoogle Scholar
Li, Y, Qiu, YY, Zeng, MH, Diao, PW, Chang, QC, Gao, Y, Zhang, Y and Wang, CR (2019) The complete mitochondrial genome of Echinostoma miyagawai: comparisons with closely related species and phylogenetic implications. Infection, Genetics and Evolution 75, 103961.CrossRefGoogle ScholarPubMed
Lie, KJ (1968) Further studies on the life history of Echinostoma lindoense Sandground and Bonne, 1940 (Trematoda: Echinostomatidae) with a report of its occurrence in Brazil. Proceedings of the Helminthological Society of Washington 35, 74–77.Google Scholar
Lie, KJ and Basch, PF (1966) Life history of Echinostoma barbosai sp. n. (Trematoda: Echinostomatidae). Journal of Parasitology 52, 1052–1057.CrossRefGoogle Scholar
Lie, KJ and Basch, PF (1967) The life history of Echinostoma paraensei sp. n. (Trematoda: Echinostomatidae). Journal of Parasitology 53, 1192–1199.CrossRefGoogle Scholar
Luton, K, Walker, D and Blair, D (1992) Comparison of ribosomal internal transcribed spacer from two congeneric species of flukes (Platyhelminthes: Trematoda: Digenea). Molecular and Biochemical Parasitology 56, 323–328.CrossRefGoogle Scholar
Lutz, A (1924) Estudos sobre a evolução dos endotrematódeos brazileiros. Memórias do Instituto Oswaldo Cruz 17, 55–57.CrossRefGoogle Scholar
Maldonado, A Jr, Loker, ES, Morgan, JAT, Rey, L and Lanfredi, RM (2001) Description of the adult worms of a new Brazilian isolate of Echinostoma paraensei (Platyhelminthes: Digenea) from its natural vertebrate host Nectomys squamipes by light and scanning electron microscopy and molecular analysis. Parasitology Research 87, 840–848.Google ScholarPubMed
Maldonado, A Jr, Vieira, GO and Lanfredi, RM (2003) Echinostoma luisreyi n. sp. (Platyhelminthes: Digenea) by light and scanning electron microscopy. Journal of Parasitology 89, 800–808.CrossRefGoogle Scholar
Mello, A (1933) Da ocorrência de Echinostoma revolutum (Fröelich, 1802) em Gallus domesticus no Brasil. Archivos da Escola Superior de Agricultura e Medicina Veterinária 10, 172.Google Scholar
Mohanta, UK, Watanabe, T, Anisuzzaman, , Ohari, Y 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 (1998a) Mitochondrial ND1 gene sequences used to identify echinostome isolates from Australia and New Zealand. Internal Journal for Parasitology 28, 493–502.CrossRefGoogle Scholar
Morgan, JAT and Blair, D (1998b) Relative merits of nuclear ribosomal internal transcribed spacers and mitochondrial CO1 and ND1 genes for distinguishing among Echinostoma species (Trematoda). Parasitology 116, 289–297.CrossRefGoogle Scholar
Nagataki, M, Tantrawatpan, C, Agatsuma, T, Sugiura, T, Duenngai, K, Sithithaworn, P, Andrews, RH, Petney, TN and Saijuntha, W (2015) Mitochondrial DNA sequences of 37 collar-spined echinostomes (Digenea: Echinostomatidae) in Thailand and Lao PDR reveals presence of two species: Echinostoma revolutum and E. miyagawai. Infection, Genetics and Evolution 35, 56–62.CrossRefGoogle ScholarPubMed
Pérez-Ponce de León, G, García-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
Pinacho-Pinacho, CD, García-Varela, M, Sereno-Uribe, AL and Pérez-Ponce de León, G (2018) A hyper-diverse genus of acanthocephalans revealed by tree-based and non-tree-based species delimitation methods: ten cryptic species of Neoechinorhynchus in Middle American freshwater fishes. Molecular Phylogenetics and Evolution 127, 30–45.CrossRefGoogle ScholarPubMed
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
Puillandre, N, Brouillet, S and Achaz, G (2021) ASAP: assemble species by automatic partitioning. Molecular Ecology Resources 21, 609–620.CrossRefGoogle ScholarPubMed
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, 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
Sandground, JH and Bonne, C (1940) Echinostoma lindoensis n. sp., a new parasite of man in the Celebes with an account of its life history and epidemiology. American Journal of Tropical Medicine and Hygiene 20, 511–535.CrossRefGoogle Scholar
Sorensen, RE, Curtis, J and Minchella, DJ (1998) Intraspecific variation in the rDNA ITS loci of 37-collar-spined echinostomes from North America: implication for sequence-based diagnoses and phylogenetics. Journal of Parasitology 84, 992–997.CrossRefGoogle Scholar
Sutton, CA and Lunaschi, L (1980) Contribución al conocimiento de la fauna parasitológica argentina VII. Nuevo digeneo en Chloephaga picta leucoptera (Gmelin). Neotropica 26, 13–17.Google Scholar
Tkach, VV, Littlewood, DTJ, Olson, PD, Kinsella, JM, Swiderski, Z (2003) Molecular phylogenetic analysis of the MicrophalloideaWard, 1901 (Trematoda: Digenea). Systematic Parasitology 56, 1–15.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, 1–15.CrossRefGoogle Scholar
Toledo, R, Muñoz-Antoli, C and Esteban, JG (2000) The life-cycle of Echinostoma friedi n. sp. (Trematoda: Echinostomatidae) in Spain and a discussion on the relationships within the ‘revolutum’ group based on cercarial chaetotaxy. Systematic Parasitology 45, 199–207.CrossRefGoogle Scholar
Toledo, R, Radev, V, Kanev, I, Gardner, SL and Fried, B (2014) History of Echinostomes (Trematoda). Acta Parasitologica 59, 553–565.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, 839–846.CrossRefGoogle ScholarPubMed
Yamaguti, S (1935) Studies on the helminth fauna of Japan. Part 5. Trematodes of birds, III. Japanese Journal of Zoology 6, 159–182.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
Supplementary material: File

Valadão et al. supplementary material

Figure S1

Download Valadão et al. supplementary material(File)
File 465.3 KB