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Trinigyrus spp. (Monogenea: Dactylogyridae) from Brazilian catfishes: new species, molecular data and new morphological contributions to the genus

Published online by Cambridge University Press:  20 February 2020

L. Franceschini Open the ORCID record for L. Franceschini [Opens in a new window] ,
A.A. Acosta Open the ORCID record for A.A. Acosta [Opens in a new window] ,
A.C. Zago Open the ORCID record for A.C. Zago [Opens in a new window] ,
M.I. Müller Open the ORCID record for M.I. Müller [Opens in a new window]  and
R.J. da Silva Open the ORCID record for R.J. da Silva [Opens in a new window]
L. Franceschini*
Affiliation:
Department of Parasitology, São Paulo State University (UNESP), Institute of Biosciences, Rua Professor Doutor Antônio Celso Wagner Zanin, 250, Botucatu, São Paulo CEP 18618-689, Brazil
A.A. Acosta
Affiliation:
Department of Parasitology, São Paulo State University (UNESP), Institute of Biosciences, Rua Professor Doutor Antônio Celso Wagner Zanin, 250, Botucatu, São Paulo CEP 18618-689, Brazil Water Research Group, Unit for Environmental Sciences and Management, Potchefstroom Campus, North-West University, Private Bag X6001, Potchefstroom 2520, South Africa
A.C. Zago
Affiliation:
Department of Parasitology, São Paulo State University (UNESP), Institute of Biosciences, Rua Professor Doutor Antônio Celso Wagner Zanin, 250, Botucatu, São Paulo CEP 18618-689, Brazil
M.I. Müller
Affiliation:
Department of Parasitology, São Paulo State University (UNESP), Institute of Biosciences, Rua Professor Doutor Antônio Celso Wagner Zanin, 250, Botucatu, São Paulo CEP 18618-689, Brazil Department of Biological Sciences, Federal University of São Paulo (Unifesp), Rua Professor Arthur Riedel, 275, Jardim Eldorado, Diadema, São Paulo 09972-270, Brazil
R.J. da Silva
Affiliation:
Department of Parasitology, São Paulo State University (UNESP), Institute of Biosciences, Rua Professor Doutor Antônio Celso Wagner Zanin, 250, Botucatu, São Paulo CEP 18618-689, Brazil
*
Author for correspondence: L. Franceschini, E-mail: [email protected]
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Abstract

This study describes two new species, Trinigyrus anthus n. sp. and Trinigyrus carvalhoi n. sp., from gills of Hypostomus spp. from the Upper Paraná River basin, Brazil. Trinigyrus peregrinus is redescribed based on examination of its holotype, paratypes and new material of specimens parasitizing Pterygoplichthys ambrosettii, also from the Upper Paraná River basin, Brazil. New morphological features were included in the diagnosis of the genus, such as the presence of a sclerotized border on the anchor base, and a weakly sclerotized fringe on the base of the male copulatory organ (MCO). Trinigyrus anthus n. sp. differs from other congeners by the shape of the MCO, presenting an enlarged base with sclerotized fringes resembling flower petals. Trinigyrus carvalhoi n. sp. and T. peregrinus are similar but can be differentiated from each other mainly by the sclerotization of the vagina (absent in the new species), and the morphology of the MCO (C-shaped versus one counterclockwise circle, respectively). For the first time, gene sequences of Trinigyrus spp. from Brazil were obtained (partial ribosomal 28S and mitochondrial cytochrome c oxidase I (mtCOI)). The genetic divergences among the new species and T. peregrinus varied from 2 to 3% (6‒18 pb) based on sequences of 28S ribosomal DNA (rDNA), and 6–7% (83‒92 pb) using mtCOI. Phylogenetic analyses based on partial 28S rDNA revealed that Trinigyrus, Heteropriapulus and Unilatus formed a monophyletic and well-supported clade of monogeneans from Neotropical freshwater loricariids, suggesting a closer relationship among these dactylogyrids and their hosts.

Keywords

DactylogyridsNeotropical regioncatfishesphylogenyhost–parasite relationships28S rDNAmtCOI
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e126
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

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References

Acosta, AA, Franceschini, L, Zago, AC, Scholz, T and Silva, RJ (2017) Six New species of Heteropriapulus (Monogenea: Dactylogyridae) from South American fishes with an amended diagnosis do the genus. Zootaxa 4290, 459–482.CrossRefGoogle Scholar
Acosta, AA, Scholz, T, Blasco-Costa, I, Alves, PV and Silva, RJ (2018) A new genus and two new species of dactylogyrids monogeneans from gills of Neotropical catfishes (Siluriformes: Doradidae and Loricariidae). Parasitology International 67, 4–12.CrossRefGoogle Scholar
Acosta, AA, Mendoza-Palmero, CA, da Silva, RJ and Scholz, T (2019) A new genus and four new species of dactylogyrids (Monogenea), gill parasites of pimelodid catfishes (Siluriformes: Pimelodidae) in South America and the reassignment of Urocleidoides megorchis Mizelle et Kritsky, 1969. Folia Parasitologica 66, 004.CrossRefGoogle ScholarPubMed
ANEEL (Agência Nacional de Energia Elétrica) (2008) Atlas de Energia Elétrica do Brasil. 3rd edn. 236 pp. Brasília, ANEEL.Google Scholar
Boeger, WA and Belmont-Jégu, E (1994) Neotropical Monogenoidea. 21. Trinigyrus mourei sp. n. (Dactylogyridae) from the gills of the Amazonian catfish Hypostomus marginatus (Loricariidae). Amazoniana 13, 13–16.Google Scholar
Boeger, WA and Kritsky, D (1993) Phylogeny and a revised classification of the Monogenoidea Bychowsky, 1937 (Platyheiminthes). Systematic Parasitology 26, 1–32.CrossRefGoogle Scholar
Boeger, WA and Vianna, RT (2006) Monogenoidea. pp. 42–116in Thatcher, VE (Ed) Amazon fish parasites. 2nd edn. Sofia, Bulgaria, Pensoft Publishers.Google Scholar
Boeger, WA, Domingues, MV and Kritsky, DC (1997) Neotropical Monogenoidea. 32. Cacatuocotyle paranaensis n. g., n. sp. (Dactylogyridae, Ancyrocephalinae) from Characidium spp. (Teleostei, Characidae) from the State of Paraná, Brazil. Systematic Parasitology 36, 75–78.CrossRefGoogle Scholar
Braga, MP, Araújo, SBL and Boeger, WA (2014) Patterns of interaction between Neotropical freshwater fishes and their gill Monogenoidea (Platyhelminthes). Parasitology Research 113, 481–490.CrossRefGoogle Scholar
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Dias, KGA, Vieira, DHMD, Camargo, AA, Silva, RJ, Azevedo, RK and Abdallah, VD (2017) Diversity of monogeneans parasites from Characiformes fishes in the Batalha river and Peixe's river, State of São Paulo, Brazil. Neotropical Helminthology 11, 317–330.Google Scholar
Eichler, W (1948) Some rules in ectoparasites. Annal and Magazine of Natural History 12, 588–598.CrossRefGoogle Scholar
Ergens, R (1969) The suitability of ammonium picrate-glycerin in preparing slides of lower Monogenoidea. Folia Parasitologica 16, 320.Google Scholar
Eschmeyer, WN, Fricke, R and van der Laan, R (Eds) (2019) Catalog of fishes: Genera, species, references. Available at http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp (accessed in 28/09/2019).Google Scholar
Franceschini, L, Zago, AC, Müller, MI, Francisco, CJ, Takemoto, RM and Silva, RJ (2018) Morphology and molecular characterization of Demidospermus spirophallus n. sp., D. prolixus n. sp. (Monogenea: Dactylogyridae) and a redescription of D. anus in siluriform catfish from Brazil. Journal of Helminthology 92, 228–243.CrossRefGoogle Scholar
Froese, R and Pauly, D (2019) FishBase. Available at http://www.fishbase.org (accessed in 28/09/2019).Google Scholar
Grande, L and Eastman, JTA (1986) A review of Antarctic ichthyofaunas in the light of new fossil discoveries. Palaeontology 29, 113–137.Google Scholar
Guindon, S and Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Hanek, G, Molnar, K and Fernando, CH (1974) Three new genera of Dactylogyridae (Monogenea) from freshwater fishes of Trinidad. Journal of Parasitology 60, 911–913.CrossRefGoogle ScholarPubMed
Humason, GL (1979) Animal tissue techniques. 4th edn. 661 pp. San Francisco, California, W.H. Freeman Co.Google Scholar
ICZN (International Commission on Zoological Nomenclature) (2012) 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
Jogunoori, W, Kritsky, DC and Venkatanarasaiah, J (2004) Neotropical Monogenoidea. 46. Three new species from the gills of introduced aquarium fishes in India, the proposal of Heterotylus n. g. and Diaphorocleidus n. g., and the reassignment of some previously described species of Urocleidoides Mizelle & Price, 1964 (Polyochoinea: Dactylogyridae). Systematic Parasitology 58, 115–124.CrossRefGoogle Scholar
Kappas, I, Vittas, S, Pantzartzi, CN, Drosopoulou, E and Scouras, ZG (2016) A time-calibrated mitogenome phylogeny of catfish (Teleostei: Siluriformes). PLoS One 11, e0166988.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, 1647–1649.CrossRefGoogle ScholarPubMed
Kimura, M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.CrossRefGoogle ScholarPubMed
Kritsky, DC and Kulo, SD (1992) Schilbetrematoides pseudodactylogyrus gen. et sp. n. (Monogenoidea, Dactylogyridae, Ancyrocephalinae) from the gills of Schilbe intermedius (Siluriformes, Schilbeidae) in Togo, Africa. Journal of the Helminthological Society of Washington 59, 195–200.Google Scholar
Kritsky, DC, Boeger, WA and Thatcher, VE (1986) Neotropical Monogenea. 9. Status of Trinigyrus Hanek, Molnar & Fernando, 1974 (Dactylogyridae) with descriptions of two new species from loricariid catfishes from the Brazilian Amazon. Proceedings of the Biological Society of Washington 99, 392–398.Google Scholar
Li, H and Huang, Q (2012) One new Chinese record genera (Ancyrocephalidae) and one new species and one new recorded of Monogenea parasiting on gills of Hypostomus plecostomus. Journal of Dalian Ocean University 27, 116–119 (in Chinese with Abstract in English).Google Scholar
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, AE, 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 Linnean Society 78, 155–171.CrossRefGoogle Scholar
Mendoza-Franco, EF, Mendoza-Palmero, CA and Scholz, T (2016) New species of Ameloblastella Kritsky, Mendoza-Franco & Scholz, 2000 and Cosmetocleithrum Kritsky, Thatcher & Boeger, 1986 (Monogenea: Dactylogyridae) infecting the gills of catfishes (Siluriformes) from the Peruvian Amazonia. Systematic Parasitology 93, 847–862.CrossRefGoogle ScholarPubMed
Mendoza-Franco, EF, Tun, MCR, Anchevida, AJD and Rodríguez, RER (2018) Morphological and molecular (28S rRNA) data of monogeneans (Platyhelminthes) infecting the gill lamellae of marine fishes in the Campeche Bank, southwest Gulf of Mexico. ZooKeys 783, 125–161.CrossRefGoogle Scholar
Mendoza-Palmero, CA, Blasco-Costa, I and Scholz, T (2015) Molecular phylogeny of Neotropical monogeneans (Platyhelminthes: Monogenea) from catfishes (Siluriformes). Parasites & Vectors 8, 164.CrossRefGoogle Scholar
Mendoza-Palmero, CA, Mendoza-Franco, EF, Acosta, AA and Scholz, T (2019) Walteriella n. g. (Monogenoidea: Dactylogyridae) from the gills of pimelodid catfishes (Siluriformes: Pimelodidae) from the Peruvian Amazonia based on morphological and molecular data. Systematic Parasitology 96, 441–452.CrossRefGoogle Scholar
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. pp. 1–8in SC10 Workshop on Gateway Computing Environments (GCE10), New Orleans, 14 November.CrossRefGoogle Scholar
Mizelle, JD and Klucka, AR (1953) Studies on monogenetic trematodes. XIV. Dactylogyridae from Wisconsin fishes. American Midland Naturalist 49, 720–733.CrossRefGoogle Scholar
Mo, T (1991) Anatomy, relationships and systematics of the Bagridae (Teleostei, Siluroidei) with a hypothesis of siluroid phylogeny. 217 pp. Koenigstein, Koeltz Scientific Books.Google Scholar
Negrelli, DC, Abdallah, VD and Azevedo, RK (2017) Metazoan parasites of the lambari Astyanax altiparanae collected in the Batalha River, State of São Paulo. Brazilian Journal of Biology 78, 535–539.CrossRefGoogle ScholarPubMed
Nelson, JS (2006) Fishes of the world. New York, John Wiley & Sons.Google Scholar
Nitta, M and Nagasawa, K (2016) Four alien monogeneans, including Trinigyrus peregrinus n. sp., parasitic on the invasive armored catfish Pterygoplichthys disjunctivus (Siluriformes: Loricariidae) from Okinawa-jima Island, Okinawa Prefecture. Japan. Species Diversity 21, 95–104.CrossRefGoogle Scholar
Plaisance, L, Rousset, V, Morand, S and Littlewood, DTJ (2008) Colonization of Pacific islands by parasites of low dispersal ability: phylogeography of two monogenean species parasitizing butterflyfishes in the South Pacific Ocean. Journal of Biogeography 35, 76–87.Google 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 Evolution 48, 369–371.CrossRefGoogle Scholar
Posada, D (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.CrossRefGoogle ScholarPubMed
Rambaut, A (2009) Molecular evolution, phylogenetics and epidemiology: Fig-Tree. Available at http//tree.bio.ed.ac.uk/software/figtree/ (accessed in 23/07/2019).Google Scholar
Ronquist, F and Huelsenbeck, JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Šimková, A, Matějusová, I and Cunningham, CO (2006) A molecular phylogeny of the Dactylogyridae sensu Kritsky & Boeger (1989) (Monogenea) based on the D1–D3 domains of the large subunit rDNA. Parasitology 133, 43–53.CrossRefGoogle ScholarPubMed
Sullivan, JP, Lundberg, JG and Hardman, MA (2006) A phylogenetic analysis of the major groups of catfishes (Teleostei: Siluriformes) using rag1 and rag2 nuclear gene sequences. Molecular Phylogenetics Evolution 41, 636–662.CrossRefGoogle 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 30, 2725–2729.CrossRefGoogle ScholarPubMed
Thatcher, VE (2006) Amazon fish parasites. 2nd edn. 508 pp. Sofia, Bulgaria, Pensoft.Google Scholar
Wang, M, Shuai, Y, Brown, CL, Shaharon-Harrison, F, Sun-fen, S and Yang, T (2014) Phylogeography of Tetrancistrum nebulosi (Monogenea, Dactylogyridae) on the host of mottled spinefoot (Siganus fuscescens) in the South China Sea, inferred from mitochondrial COI and ND2 genes. Mitochondrial DNA 27, 1–11.Google ScholarPubMed
Wu, XY, Zhu, XQ, Xie, MQ and Li, AX (2006) The radiation of Haliotrema (Monogenea: Dactylogyridae: Ancyrocephalinae): molecular evidence and explanation inferred from LSU rDNA sequences. Parasitology 132, 659–668.CrossRefGoogle ScholarPubMed
Xia, X (2013) DAMBE5: a comprehensive software package for data analysis in molecular biology and evolution. Molecular Biology and Evolution 30, 1720–1728.CrossRefGoogle ScholarPubMed
Yamada, FH, Acosta, AA, Yamada, POF, Scholz, T and Silva, RJ (2018) A new species of Aphanoblastella Kritsky, Mendoza-Franco and Scholz, 2000 (Monogenea, Dactylogyridae) parasitic of heptapterid catfish (Siluriformes) in the Neotropical Region. Acta Parasitologica 63, 772–780.CrossRefGoogle ScholarPubMed
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