Hostname: page-component-76fb5796d-45l2p Total loading time: 0 Render date: 2024-04-28T03:17:25.570Z Has data issue: false hasContentIssue false

A new species of Creptotrematina (Trematoda: Allocreadiidae) from characid fishes of Brazil: morphological and molecular data

Published online by Cambridge University Press:  16 June 2020

K.G. Alves Dias*
Affiliation:
Laboratório de Parasitologia de Animais Silvestres, Departamento de Parasitologia, Instituto de Biociências de Botucatu, Universidade Estadual Paulista ‘Júlio de Mesquita Filho’ (UNESP) – Campus Botucatu, Botucatu, São Paulo, Brazil
G. Pérez-Ponce de León
Affiliation:
Instituto de Biología, Universidad Nacional Autónoma de México (UNAM), Ciudad de México, Mexico Escuela Nacional de Estudios Superiores Unidad Mérida (ENES)-UNAM, Km 4.5 Carretera Mérida-Tetiz, Ucú, Yucatán, Mexico
A. de Almeida Camargo
Affiliation:
Laboratório de Parasitologia de Animais Silvestres, Departamento de Parasitologia, Instituto de Biociências de Botucatu, Universidade Estadual Paulista ‘Júlio de Mesquita Filho’ (UNESP) – Campus Botucatu, Botucatu, São Paulo, Brazil
M.I. Müller
Affiliation:
Programa de Pós-Graduação em Ecologia e Evolução, Universidade Federal de São Paulo, São Paulo, Brazil
R.J. da Silva
Affiliation:
Laboratório de Parasitologia de Animais Silvestres, Departamento de Parasitologia, Instituto de Biociências de Botucatu, Universidade Estadual Paulista ‘Júlio de Mesquita Filho’ (UNESP) – Campus Botucatu, Botucatu, São Paulo, Brazil
R. Kozlowiski de Azevedo
Affiliation:
Docente do Programa de Pós-graduação em Análise de Sistemas Ambientais, Centro Universitário CESMAC, Maceió, Alagoas, Brazil
V.D. Abdallah
Affiliation:
Docente do Programa de Pós-graduação em Análise de Sistemas Ambientais, Centro Universitário CESMAC, Maceió, Alagoas, Brazil
*
Author for correspondence: K.G. Alves Dias, E-mail: karinanuros@gmail.com

Abstract

A new species of Creptotrematina Yamaguti, 1954 was collected from characid fishes, Astyanax fasciatus (Cuvier, 1819) and Astyanax lacustris Lucerna & Soares, 2016 from the Batalha River in the State of Sao Paulo, Brazil. The new species most closely resembles Creptotrematina aguirrepequenoi, but differs by the elongated shape of vitelline follicles, the extension of these follicles in the posterior end of body and the fact that they are not confluent. The morphological differences were confirmed through molecular data. Three specimens were sequenced, and molecular analyses were based on the internal transcribed spacers 2 and D1–D3 domains of the 28S ribosomal RNA gene. The obtained topologies showed the new species as a sister taxon of C. aguirrepequenoi, a species originally described from Astyanax mexicanus in Mexico, and later found in Astyanax aeneus in Costa Rica. Isolates of the new species are reciprocally monophyletic, and genetic distance values are similar to those observed in other species pairs within Allocreadiidae. These findings corroborate that the genus Creptotrematina is mostly a parasite of characids, and widely extended across the Americas, with representative species occurring between Argentina and northern Mexico.

Type
Research Paper
Copyright
Copyright © The Author(s), 2020. 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

Astrin, JJ, Zhou, X and Misof, B (2013) The importance of biobanking in molecular taxonomy, with proposed definitions for molecular vouchers in a molecular context. Zookeys 365, 6770.CrossRefGoogle Scholar
Baumgartner, G, Pavanelli, CS, Baumgartner, D, Bifi, AG, Debona, T and Frana, VA (2012) Peixes do baixo Rio Iguaçu. p. 203. Maringá, Eduem.CrossRefGoogle Scholar
Bowles, J, Blair, D and McManus, DP (1995) A molecular phylogeny of the human schistosomes. Molecular Phylogenetics and Evolution 4, 103109.CrossRefGoogle ScholarPubMed
Caira, JN and Bogéa, T (2005) Family Allocreadiidae Looss 1902. pp. 417436in Jones, A, Bray, RA and Gibson, DI (Eds) Keys to the Trematoda, vol. 2. Wallingford and London, UK, CABI Publishing and The Natural History Museum.CrossRefGoogle Scholar
Choudhury, A, Rosas-Valdez, R, Johnson, RC, Hoffman, B and Pérez-Ponce de León, G (2007) The phylogenetic position of the Allocreadiidae (Trematoda: Digenea) using partial sequences of the 18S and 28S ribosomal genes. Journal of Parasitology 93, 192196.CrossRefGoogle Scholar
Choudhury, A, García-Varela, M and Pérez-Ponce de León, G (2017) Parasites of freshwater fishes and the great American biotic interchange: a bridge too far? Journal of Helminthology 91, 174196.CrossRefGoogle ScholarPubMed
Curran, SS, Tkach, VV and Overstreet, RM (2006) A review of Polylekithum Arnold, 1934 and its familial affinities using morphological and molecular data, with description of Polylekithum catahoulensis sp. nov. Acta Parasitology 51, 238248.Google Scholar
Curran, SS, Tkach, VV and Overstreet, RM (2011) Phylogenetic affinities of Auriculostoma (Digenea: Allocreadiidae), with descriptions of two new species from Peru. Journal of Parasitology 97, 661670.CrossRefGoogle Scholar
Curran, SS, Pulis, EE, Hugg, DO, Brown, JP, Manuel, LC and Overstreet, RM (2012) Phylogenetic position of Creptotrema funduli in the Allocreadiidae based on partial 28S rDNA sequences. Journal of Parasitology 98, 873875.CrossRefGoogle ScholarPubMed
Dias, KGA, Mueller, MI, Almeida, AC, Silva, RJ, Azevedo, RK, Pérez-Ponce de Leon, G and Abdallah, VD (2018) A new species of Wallinia Pearse, 1920 (Digenea: Allocreadiidae) collected from Astyanax fasciatus (Cuvier, 1819) and A. Lacustris Lucena and Soares, 2016 (Characiformes: Characidae) in Brazil based on morphology and DNA sequences. Parasitology Research 117, 28472854.CrossRefGoogle Scholar
Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 17921797.CrossRefGoogle ScholarPubMed
Eschmeyer, WN (2020) Catalog of fishes: genera, species reference. Available at http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp (accessed May 2020).Google Scholar
Freitas, JFT (1941) Novo Trematódio parasito de peixe do rio Miranda. Revista Brasileira de Biologia 3, 249251.Google Scholar
Hamann, MI (1983) Digenea parasites of freshwater fishes in northeastern Argentina (Trematoda – Digenea). Scientific Papers of CECOAL 16, 18.Google Scholar
Hernandez-Mena, DI, Lynggaard, C, Mendoza-Garfias, B and Peréz-Ponce de Leon, G (2018) A new species of Auriculostoma (Trematoda: Allocreadiidae) from the intestine of Brycon guatemalensis (Characiformes: Bryconidae) from the Usumacinta River Basin, Mexico, based on morphology and 28S rDNA sequences, with a key to species of the genus. Zootaxa 2, 261277.Google Scholar
Jousson, O, Bartoli, P, Zaninetti, L and Pawlowski, J (1998) Use of the ITS rDNA for elucidation of some life-cycles of Mesometridae (Trematoda, Digenea). International Journal for Parasitology 28, 14031411.CrossRefGoogle Scholar
Kearse, M, Moir, R, Wilson, A, et al. (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 16471649.CrossRefGoogle ScholarPubMed
Kohn, A, Fernandes, BMM and Cohen, SC (2007) South American trematodes parasites of fishes. 318 pp. Rio de Janeiro, Imprinta Express.Google Scholar
Looss, A (1902) Ueber neue und bekannte Trematoden aus Seeschildkröten: Nebst Erörterungen zur Systematik und Nomenclatur 16, 411–894.Google Scholar
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 1–8. https://doi:10.1109/GCE.2010.5676129.CrossRefGoogle Scholar
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, 609615.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, 733755.CrossRefGoogle Scholar
Ornelas-García, CP, Domínguez-Domínguez, O and Doadrio, I (2008) Evolutionary history of the fish genus Astyanax Baird & Girard (1854) (Actinopterygii, Characidae) in Mesoamerica reveals multiple morphological homoplasies. BMC Evolutionary Biology 8, 340.CrossRefGoogle ScholarPubMed
Pérez-Ponce de León, G and Choudhury, A (2010) Parasite inventories and DNA-based taxonomy: lessons from helminths of freshwater fishes in a megadiverse country. Journal of Parasitology 96, 236244.CrossRefGoogle Scholar
Pérez-Ponce de León, G and Hernández-Mena, DI (2019) Testing the higher-level phylogenetic classification of Digenea (Platyhelminthes, Trematoda) based on nuclear rDNA sequences before entering the age of the ‘next-generation’ tree of life. Journal of Helminthology 93, 260276.CrossRefGoogle ScholarPubMed
Pérez-Ponce de León, G and Nadler, SA (2010) What we don't recognize can hurt us: a plea for awareness about cryptic species. Journal of Parasitology 96, 453464.CrossRefGoogle Scholar
Pérez-Ponce de León, G, Choudhury, A, Rosas-Valdez, R and Mejía-Madrid, H (2007) The systematic position of Wallinia spp. and Margotrema spp. (Digenea), parasites of Middle-American and Neotropical freshwater fishes, based on the 28S ribosomal RNA gene. Systematic Parasitology 68, 4955.CrossRefGoogle Scholar
Pérez-Ponce de León, G, Razo-Mendivil, U, Mendoza-Garfias, B, Rubio-Godoy, M and Choudhury, A (2015) A new species of Wallinia Pearse, 1920 (Digenea: Allocreadiidae) in Astyanax mexicanus (Characidae) from Mexico revealed by morphology and sequences of the 28S ribosomal RNA gene. Folia Parasitology 62, 18–24.Google Scholar
Pérez-Ponce de León, G, Pinacho-Pinacho, CD, Mendoza-Garfias, B, Choudhury, A and Garcia-Varela, M (2016) Phylogenetic analysis using the 28S rRNA gene reveals that the genus Paracreptotrema Choudhury, Pérez-Ponce de Leon, Brooks and Daverdin, 2006 (Digenea: Allocreadiidae) is not monophyletic; description of two new genera and one new species. Journal of Parasitology 102, 131142.CrossRefGoogle Scholar
Petkeviciute, R, Stunzenas, V, Staneviciute, G and Sokolov, SG (2010) Comparison of the developmental stages of some European allocreadiid trematode species and a clarification of their life-cycles based on ITS2 and 28S sequences. Systematic Parasitology 76, 169178.CrossRefGoogle Scholar
Rambaut, A (2009) Molecular evolution, phylogenetics and epidemiology: fig-tree. Available at http//tree.bio.ed.ac.uk/software/figtree, 06/06/2020.Google Scholar
Razo-Mendivil, U, Vázquez-Domínguez, E, Rosas-Valdez, R, Pérez-Ponce de León, G and Nadler, SA (2010) Phylogenetic analysis of nuclear and mitochondrial DNA reveals a complex of cryptic species in Crassicutis cichlasomae (Digenea: Apocreadiidae), a parasite of Middle-American cichlids. International Journal for Parasitology 70, 471486.CrossRefGoogle Scholar
Razo-Mendivil, U, Mendoza-Garfias, B, Pérez-Ponce de Leon, G and Rubio-Godoy, M (2014a) A new species of Auriculostoma (Digenea: Allocreadiidae) in the Mexican tetra Astyanax mexicanus (Actinopterygii: Characidae) from central Veracruz, Mexico, described with the use of morphological and molecular data. Journal of Parasitology 100, 331337.CrossRefGoogle Scholar
Razo-Mendivil, U, Pérez-Ponce de Leon, G and Rubio-Godoy, M (2014b) Testing the systematic position and relationships of Paracreptotremaheterandriae within the Allocreadiidae through partial 28 s rRNA gene sequences. Journal of Parasitology 100, 537541.CrossRefGoogle Scholar
Ronquist, F, Teslenko, M, Mark, P, et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 14.CrossRefGoogle ScholarPubMed
Silva, DA, Pessoa, EKR, Costa, SAGL, Chellappa, NT and Chellappa, S (2012) Ecologia alimentar de Astyanax lacustris (Osteichthyes: Characidae) na Lagoa do Piató, Assú, Rio Grande do Norte, Brasil. Biota Amazônia 2, 7484.CrossRefGoogle Scholar
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9), 1312–1313.Google Scholar
Tamura, K and Nei, M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512526.Google ScholarPubMed
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 12, 27252729.CrossRefGoogle Scholar
Uieda, VS, Buzzato, P and Kikuchi, RM (1997) Partilha de recursos alimentares em peixes em um riacho de serra do Sudeste do Brasil. Anais da Academia Brasileira de Ciências 69, 243252.Google Scholar
Xia, X (2013) DAMBE5: a comprehensive software package for data analysis in molecular biology and evolution. Molecular Biology and Evolution 30, 17201728.CrossRefGoogle ScholarPubMed
Yamaguti, S (1958) Systema helminthum. Vol I. The digenetic trematodes of vertebrates. xi + 1575pp. New York & London.Google Scholar
Yamaguti, S (1971) Synopsis of digenetic trematodes of vertebrates. Vol. I, 1074pp.; Vol II, 349 pls. Keigaku, Tokyo.Google Scholar
Supplementary material: PDF

Alves Dias et al. supplementary material

Alves Dias et al. supplementary material 1

Download Alves Dias et al. supplementary material(PDF)
PDF 28.7 KB

Alves Dias et al. supplementary material

Alves Dias et al. supplementary material 2

Download Alves Dias et al. supplementary material(Video)
Video 37.9 MB

Alves Dias et al. supplementary material

Alves Dias et al. supplementary material 3

Download Alves Dias et al. supplementary material(Video)
Video 8.2 MB

Alves Dias et al. supplementary material

Alves Dias et al. supplementary material 4

Download Alves Dias et al. supplementary material(Video)
Video 18.2 MB