Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-22T10:21:25.513Z Has data issue: false hasContentIssue false

Morphological and genetic description of Moniliformis necromysi sp. n. (Archiacanthocephala) from the wild rodent Necromys lasiurus (Cricetidae: Sigmondontinae) in Brazil

Published online by Cambridge University Press:  19 March 2020

A.P.N. Gomes
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, 4365 Avenida Brasil, Manguinhos, Rio de Janeiro, RJ, 21045-900, Brazil Post-Graduate Program in Parasite Biology of Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro, RJ, 21040-360, Brazil
N.A. Costa
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, 4365 Avenida Brasil, Manguinhos, Rio de Janeiro, RJ, 21045-900, Brazil
R. Gentile
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, 4365 Avenida Brasil, Manguinhos, Rio de Janeiro, RJ, 21045-900, Brazil
R.V. Vilela*
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, 4365 Avenida Brasil, Manguinhos, Rio de Janeiro, RJ, 21045-900, Brazil
A. Maldonado Jr
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, 4365 Avenida Brasil, Manguinhos, Rio de Janeiro, RJ, 21045-900, Brazil
*
Author for correspondence: R.V. Vilela, E-mail: [email protected]

Abstract

A new species of Moniliformis Travassos, 1915 (Acanthocephala: Moniliformidae) is described from the hairy-tailed bolo mouse, Necromys lasiurus Lund, 1840 (Cricetidae: Sigmondontinae), captured in the Brazilian Cerrado, in Uberlândia, state of Minas Gerais, Brazil. The specimens were studied by light and scanning electron microscopy. Molecular phylogenies were inferred from partial nuclear large subunit ribosomal RNA gene sequences and partial mitochondrial cytochrome c oxidase subunit I gene. The new species is distinguished from other moniliformid species by the number of rows and number of hooks per row, size of the proboscis, size of the eggs, host species and geographical distribution. Molecular phylogenies and genetic distances analyses demonstrated that Moniliformis necromysi sp. n. forms a well-supported monophyletic group with sequences of other species of Moniliformis and is distinguished from them, which agrees with the morphological characteristics, allocating the new species to this genus and to the family Moniliformidae Van Cleave, 1924. This is the first moniliformid acanthocephalan described from a wild rodent in Brazil.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2020

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

Abascal, F, Zardoya, R and Telford, MJ (2010) TranslatorX: multiple alignments of nucleotide sequences guided by amino acid translations. Nucleic Acids Research 38, 713.CrossRefGoogle ScholarPubMed
Amato, JFR (1985) Manual de Técnicas para a Preparação de Coleções Zoológicas. 8. Platelmintos (temnocefálidos, trematódeos, cestóides, cestodários) e acantocéfalos. São Paulo, Sociedade Brasileira de Zoologia.Google Scholar
Amin, OM (1985) Classification. pp. 2772in Crompton, DWT and Nickol, BB (Eds) Biology of the acanthocephala. London, Cambridge University Press.Google Scholar
Amin, OM (1987) Key to the families and subfamilies of Acanthocephala with the erection of a new class (Polyacanthocephala) and a new order (Polyacanthorhynchida). Journal of Parasitology 73, 12161219.CrossRefGoogle Scholar
Amin, OM (2013) Classification of the Acanthocephala. Folia Parasitologica 60, 273305.CrossRefGoogle ScholarPubMed
Amin, OM, Evans, P, Heckmann, RA and El-Naggar, AM (2013) The description of Mediorhynchus africanus n. sp. (Acanthocephala: Gigantorhynchidae) from galliform birds in Africa. Parasitology Research 112, 2897–906.CrossRefGoogle ScholarPubMed
Amin, OM, Heckmann, RA, Halajian, A, El-Naggar, A and Takavol, S (2014) Description of Moniliformis kalahariensis (Acanthocephala: Moniliformidae) from the South African hedgehog Atelerix frontalis (Erinaceidae) in South Africa. Comparative Parasitology 81, 3343.CrossRefGoogle Scholar
Amin, OM, Heckmann, RA, Mohammed, O and Evans, RP (2016) Morphological and molecular descriptions of Moniliformis saudi sp. n. (Acanthocephala: Moniliformidae) from the desert hedgehog, Paraechinus aethiopicus (Ehrenberg) in Saudi Arabia, with a key to species and notes on histopathology. Folia Parasitologica 63, 014.CrossRefGoogle Scholar
Amin, OM, Heckmann, RA, Sharifdini, M and Albayati, NY (2019) Moniliformis cryptosaudi n. sp. (Acanthocephala: Moniliformidae) from the long-eared hedgehog Hemiechinus auritus (Gmelin) (Erinaceidae) in Iraq; a case of incipient cryptic speciation related to M. saudi in Saudi Arabia. Acta Parasitologica 64, 195204.CrossRefGoogle Scholar
Anderson, RC, Chabaud, AG and Willmott, S (2009) Keys to the nematode parasites of vertebrates: archival volume. Wallingford, CAB International.CrossRefGoogle Scholar
Anisimova, M and Gascuel, O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Systematic Biology 55, 539552.CrossRefGoogle ScholarPubMed
Araújo, EO, Mendes, MM, Langone, PQ and Müller, G (2014) The helminth parasites of Rattus rattus (Linnaeus, 1758) of urban, intermediate and rural environments in southern Brazil. Neotropical Helminthology 8, 1922.Google Scholar
Berenji, F, Fata, A and Hosseininejad, Z (2007) A case of Moniliformis moniliformis (Acanthocephala) infection in Iran. Korean Journal of Parasitology 45, 145148.CrossRefGoogle ScholarPubMed
Bonvicino, CR, Oliveira, JA and D'Andrea, PS (2008) Guia dos roedores do Brasil, com chave para gêneros baseadas em caracteres externos. pp. 120. Rio de Janeiro, Centro Pan-Americano de Febre Aftosa – OPAS/OMS.Google Scholar
Cardoso, TS, Simões, RO, Luque, JLF, Maldonado, A Jr and Gentile, R (2016) The influence of habitat fragmentation on helminth communities in rodent populations from a Brazilian mountain Atlantic forest. Journal of Helminthology 90, 460468.CrossRefGoogle ScholarPubMed
Chisholm, LA, Morgan, JA, Adlard, RD and Whittington, ID (2001) Phylogenetic analysis of the Monocotylidae (Monogenea) inferred from 28S rDNA sequences. International Journal for Parasitology 31, 12531263.CrossRefGoogle ScholarPubMed
Costa, NA, Simões, RO, Vilela, RV, Souza, JGR, Cardoso, ST, Leiner, NO, Gentile, R and Maldonado, A Jr (2018) Morphological and genetic characterization of Pterygodermatites (Paucipectines) zygodontomis (Nematoda: Rictulariidae) from Necromys lasiurus (Rodentia: Sigmodontinae) from Uberlândia, Brazil. Journal of Helminthology 92, 618629.CrossRefGoogle ScholarPubMed
Falla, AC, Brieva, C and Bloor, P (2015) Mitochondrial DNA diversity in the acanthocephalan Prosthenorchis elegans in Colombia based on cytochrome c oxidase I (COI) gene sequence. International Journal for Parasitology: Parasites and Wildlife 4, 401407.Google ScholarPubMed
Folmer, O, Black, M, Hoeh, W, Lutz, R and Vrijenhoek, R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294299.Google ScholarPubMed
García-Varela, M and Nadler, AS (2005) Phylogenetic relationships of Palaeacanthocephala (Acanthocephala) inferred from SSU and LSU rDNA gene sequences. Journal of Parasitology 91, 14011409.CrossRefGoogle ScholarPubMed
García-Varela, M and Pérez-Ponce de León, P (2015) Advances in the classification of acanthocephalans: evolutionary history and evolution of the parasitism. pp. 182201in Morand, S, Krasnov, BR and Littlewood, DTJ (Eds) Parasite diversity and diversification: evolutionary ecology meets phylogenetics. Cambridge, University Press.CrossRefGoogle Scholar
Gazi, M, Sultana, T, Min, GS, Park, YC, García-Varela, M, Nadler, SA and Park, JK (2012) The complete mitochondrial genome sequence of Oncicola luehei (Acanthocephala: Archiacanthocephala) and its phylogenetic position within Syndermata. Parasitology International 61, 307316.CrossRefGoogle ScholarPubMed
Gazi, M, Kim, J, García-Varela, M, Park, C, Littlewood, D, Tim, J and Park, J (2016) Mitogenomic phylogeny of Acanthocephala reveals novel class relationships. Zoologica Scripta 45, 437454.CrossRefGoogle Scholar
Gibson, DI and McCarthy, TJ (1987) Bats as hosts of acanthocephalan parasites. Helminthological Abstracts Series A 56, 159162.Google Scholar
Guindon, S, Dufayard, JF, Lefort, V, Anisimova, M, Hordijk, W and Gascuel, O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307321.CrossRefGoogle ScholarPubMed
Hassouna, N, Michot, B and Bachellerie, JP (1984) The complete nucleotide sequence of mouse 28S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eukaryotes. Nucleic Acids Research 12, 35633583.CrossRefGoogle ScholarPubMed
Jukes, TH and Cantor, CR (1969) Evolution of protein molecules. pp. 21132in Munro, HN (Ed) Mammalian protein metabolism. New York, Academic Press.CrossRefGoogle Scholar
Kamimura, K, Yonemitsu, K, Maeda, K, Sakaguchi, S, Setsuda, A, Varcasia, A and Sato, H (2018) An unexpected case of a Japanese wild boar (Sus scrofa leucomystax) infected with the giant thorny-headed worm (Macracanthorhynchus hirudinaceus) on the mainland of Japan (Honshu). Parasitology Research 117, 23152322.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
Lefort, V, Longueville, JE and Gascuel, O (2017) SMS: Smart Model Selection in PhyML. Molecular Biology and Evolution 34, 24222424.CrossRefGoogle ScholarPubMed
Limongi, JE, Moreira, FG, Peres, JB, Suzuki, A, Ferreira, IB, Souza, RP, Pinto, RMC and Pereira, LE (2013) Serological survey of hantavirus in rodents in Uberlândia, Minas Gerais, Brazil. Revista Instituto de Medicina Tropical 55, 155158.CrossRefGoogle ScholarPubMed
López-Caballero, J, Mata-López, R, García-Varela, M and Pérez-Ponce de León, G (2015) Genetic variation of Oligacanthorhynchus microcephalus (Acanthocephala: Archiacanthocephala: Oligacanthorhynchidae), parasite of three species of opossums (Mammalia: Didelphidae) across central and southeastern Mexico. Comparative Parasitology 82, 175186.CrossRefGoogle Scholar
Machado Filho, DA (1946) Sobre Moniliformis moniliformis (Bremser), Moniliformis travassosi Meyer, 1932 e outras especes duvidosas do gênero (Acanthocephala). Boletim Escola Nacional Veterinária, Rio de Janeiro 1, 1327.Google Scholar
Maddison, WP and Maddison, DR (2018) Mesquite: a modular system for evolutionary analysis. Version 3.51. Available at http://www.mesquiteproject.org. Accessed 14 September 2018.Google Scholar
Martins, NB, Del Rosario Robles, M and Navone, GT (2017) A new species of Moniliformis from a Sigmodontinae rodent in Patagonia (Argentina). Parasitology Research 116, 20912099.CrossRefGoogle Scholar
Mendenhall, IH, Ch'ng, L, Neves, ES, Borthwick, SA and Smith, GJD (2018) High diversity of medically important gastrointestinal rodent-borne helminths in Singapore. Zoonoses Public Health 65, 361366.CrossRefGoogle ScholarPubMed
Meyers, WM, Neafie, RC, Marty, AM and Wear, DJ (2000) Pathology of infectious diseases. pp. 519529. Vol. 1, Helminthiasis. Armed Forces Institute of Pathology and American Registry of Pathology, Washington, DC.Google Scholar
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. pp. 18 in Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA. 2010 November 14.CrossRefGoogle Scholar
Pan, TS and Nie, P (2013) The complete mitochondrial genome of Pallisentis celatus (Acanthocephala) with phylogenetic analysis of acanthocephalans and rotifers. Folia Parasitologica 60, 181191.CrossRefGoogle ScholarPubMed
Passamaneck, Y and Halanych, KM (2006) Lophotrochozoan phylogeny assessed with LSU and SSU data: evidence of lophophorate polyphyly. Molecular Phylogenetic and Evolution 40, 2028.CrossRefGoogle ScholarPubMed
Rambaut, A, Drummond, AJ, Xie, D, Baele, G and Suchard, MA (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901904.CrossRefGoogle Scholar
Redford, K and Eisenberg, J (1999) Mammals of the neotropics. 3rd edn. Chicago, The University of Chicago Press.Google Scholar
Ronquist, F, Teslenko, M, van der Mark, P, et al. (2012) MrBayes version 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539542.CrossRefGoogle ScholarPubMed
Salehabadi, A, Mowlavi, G and Sadjjadi, SM (2008) Human infection with Moniliformis moniliformis (Bremser, 1811) (Travassos, 1915) in Iran: another case report after three decades. Vector Borne Zoonotic Disease 8, 101103.CrossRefGoogle ScholarPubMed
Santos, CP and Gibson, DI (2015) Checklist of the helminth parasites of South American bats. Zootaxa 3937, 471499.CrossRefGoogle ScholarPubMed
Santos, EGN, Chame, M, Chagas-Moutinho, VA and Santos, CP (2017) Morphology and molecular analysis of Oncicola venezuelensis (Acanthocephala: Oligacanthorhynchidae) from the ocelot Leopardus pardalis in Brazil. Journal of Helminthology 91, 605612.CrossRefGoogle ScholarPubMed
Schmidt, GD (1972) Revision of the class Archiacanthocephala Meyer, 1931 (Phylum Acanthocephala), with emphasis on Oliganthorhynchidae Southwell et Macfie, 1925. Journal of Parasitology 58, 290297.CrossRefGoogle Scholar
Simões, RO, Gentile, R, Rademaker, V, D'Andrea, PS, Herrera, H, Freitas, T, Lanfredi, R and Maldonado, A Jr (2010) Variation in the helminth community structure of Thrichomys pachyurus (Rodentia: Echimyidae) in two sub-regions of the Brazilian Pantanal: the effects of land use and seasonality. Journal of Helminthology 84, 266275.CrossRefGoogle ScholarPubMed
Simões, RO, Souza, JGR, Maldonado, A Jr and Luque, JL (2011) Variation in the helminth community structure of three sympatric sigmodontine rodents from the coastal Atlantic Forest of Rio de Janeiro, Brazil. Journal of Helminthology 85, 171178.CrossRefGoogle ScholarPubMed
Simões, RO, Maldonado, A Jr and Luque, JL (2012) Helminth communities in three sympatric rodents from the Brazilian Atlantic Forest: contrasting biomass and numerical abundance. Brazilian Journal of Biology 72, 909914.CrossRefGoogle ScholarPubMed
Simões, RO, Garcia, JS, Costa-Neto, SF, Santos, MM, Faro, MJ and Maldonado, A Jr (2017) Survey of helminths in small mammals along the aqueduct of the São Francisco river in the caatinga biome. Oecologia Australis 21, 8892.CrossRefGoogle Scholar
Southwell, T and Macfie, JWS (1925) On a collection of Acanthocephala in the Liverpool School of Tropical Medicine. Annals Tropical Medicine Parasitology 19, 141284.CrossRefGoogle Scholar
Swofford, DL (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) Version 4. 468. Massachusetts, Sinauer Associates Sunderland.Google Scholar
Tavares, LER, Campião, KM, Costa-Pereira, R and Paiva, F (2017) Helmintos endoparasitos de vertebrados silvestres em Mato Grosso do Sul. Brasil Iheringia Série Zoologia 107, e2017106.Google Scholar
Tietz Marques, SM and Scroferneker, ML (2003) Gastrointestinal helminth parasites of the black rat (Rattus rattus) in a coal mine in Minas do Leão, RS, Brazil. Revista Ciências Agroveterinária 2, 140142.Google Scholar
Travassos, L (1915) Revisão dos Acanthocephalos Brasileiros. I. Fam. Gigantorthynchidae Hamann, 1982 (Nota prévia). Brasil Médico 29, 105.Google Scholar
Travassos, L (1917) Contribuição para o conhecimento da fauna helmintológica brasileira, XVII. Revisão dos acantocéfalos brasileiros. Parte I. Fam. Gigantorhynchidae Hamann, 1982. Memórias do Instituto Oswaldo Cruz 9, 562.CrossRefGoogle Scholar
Van Cleave, HJ (1923) A key to the genera of Acanthocephala. Transactions of the American Microscopical Society 12, 184191.CrossRefGoogle Scholar
Van Cleave, HJ (1924) A critical study of the Acanthocephala described and identified by Joseph Leidy. Proceedings of the Academy of Natural Sciences of Philadelphia 76, 279334.Google Scholar
Van Cleave, HJ (1953) Acanthocephala of North American mammals. Ill. Biology Monograph 23, 179.Google Scholar
Vicente, JJ, Rodrigues, HO, Gomes, DC and Pinto, RM (1997) Nematóides do Brasil. Parte V: nematóides de mamíferos. Revitsa Brasileira de Zoologia 14(suppl. 1), 1452.CrossRefGoogle Scholar
Vieira, EM, Baumgartem, LC, Paise, G and Becker, RG (2010) Seasonal patterns and influence of temperature on the daily activity of the diurnal neotropical rodent Necromys lasiurus. Canadian Journal Zoology 88, 259265.CrossRefGoogle Scholar
Weber, M, Wey-Fabrizius, AR, Podsiadlowski, L, Witek, A, Schill, RO, Sugár, L, Herlyn, H and Hankeln, T (2013) Phylogenetic analyses of endoparasitic Acanthocephala based on mitochondrial genomes suggest secondary loss of sensory organs. Molecular Phylogenetic Evolution 66, 182189.CrossRefGoogle ScholarPubMed
Xia, X (2018) DAMBE7: new and improved tools for data analysis in molecular biology and evolution. Molecular Biology and Evolution 35, 15501552.CrossRefGoogle ScholarPubMed
Xia, X and Lemey, P (2009) Assessing substitution saturation with DAMBE. The phylogenetic handbook. pp. 615630. Cambridge, Cambridge University Press.Google Scholar
Xia, X, Xie, Z, Salemi, M, Chen, L and Wang, Y (2003) An index of substitution saturation and its application. Molecular Phylogenetics and Evolution 26, 17.CrossRefGoogle ScholarPubMed
Yamaguti, S (1963) Systema Helminthum. Vol. V. Acanthocephala. pp. 423. New York, John Wiley and Sons Interscience Publishers.Google Scholar
Supplementary material: File

Gomes et al. supplementary material

Gomes et al. supplementary material

Download Gomes et al. supplementary material(File)
File 14.5 KB