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Morphological and molecular characterization of Trichuris muris (Nematoda: Trichuridae): studies from two commensal rodent species

Published online by Cambridge University Press:  18 April 2023

J.A. Panti-May ,
M.Á. Gómez Muñoz ,
A.B. Yeh-Gorocica ,
S. Hernández-Betancourt ,
F. Milano ,
C. Galliari  and
M. R. Robles Open the ORCID record for M. R. Robles [Opens in a new window]
J.A. Panti-May
Affiliation:
Centro de Investigaciones Regionales ʻDr Hideyo Noguchi’, Universidad Autónoma de Yucatán, Yucatán, México;
M.Á. Gómez Muñoz
Affiliation:
Laboratorio Biología de los Parásitos, Facultad de Ciencias Exactas y Naturales y Agrimensura, Universidad Nacional del Nordeste, Corrientes, Argentina;
A.B. Yeh-Gorocica
Affiliation:
Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Yucatán, Mérida, México
S. Hernández-Betancourt
Affiliation:
Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Yucatán, Mérida, México
F. Milano
Affiliation:
Laboratorio Biología de los Parásitos, Facultad de Ciencias Exactas y Naturales y Agrimensura, Universidad Nacional del Nordeste, Corrientes, Argentina;
C. Galliari
Affiliation:
Centro de Estudios Parasitológicos y de Vectores CEPAVE (CCT-CONICET- La Plata), Universidad Nacional de La Plata (UNLP), Buenos Aires, Argentina
M. R. Robles*
Affiliation:
Centro de Estudios Parasitológicos y de Vectores CEPAVE (CCT-CONICET- La Plata), Universidad Nacional de La Plata (UNLP), Buenos Aires, Argentina
*
Corresponding author: M.R. Robles; E-mail: rosario@cepave.edu.ar
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Abstract

In this paper we re-describe Trichuris muris based on morphological data following isolation from two commensal rodent species, Mus musculus from Mexico and Rattus rattus from Argentina. Furthermore, we provide a molecular characterization based on mitochondrial (cytochrome c oxidase subunit 1 mitochondrial gene) and nuclear (internal transcribed spacer 2 region) markers in order to support the taxonomic identification of the studied specimens of T. muris from M. musculus. We distinguished T. muris from 29 species of Trichuris found in American rodents based on morphological and biometrical features, such as the presence of a spicular tube, length of spicule, size of proximal and distal cloacal tube and non-protrusive vulva. We suggest that spicular tube patterns can be used to classify Trichuris species in three groups. Considering that the diagnosis among the species of this genus is mainly based on morphometry, this proposal represents a relevant contribution. We provide molecular studies on two markers, making this the first contribution for T. muris in the Americas. This study makes an important contribution to the integrative taxonomy of cosmopolitan nematode species, and its correct determination from the parasitological study of commensal rodents.

Keywords

integrative taxonomyNorth AmericarodentsSouth Americawhipworms
Type
Research Paper
Information
Journal of Helminthology , Volume 97 , 2023 , e38
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally to the work.

References

Babero, BB and Murua, RB (1987) The helminth fauna of Chile. X. A new species of whipworm from a Chilean rodent. Transactions of the American Microscopical Society 106(2), 190–193.CrossRefGoogle Scholar
Babero, BB and Murua, RB (1990) A new species of whipworm from a South American hystricomorph rodent. Memórias do Instituto Oswaldo Cruz 85(2), 211–213.CrossRefGoogle Scholar
Babero, BB, Cattan, PE and Cabello, C (1975) Trichuris bradleyi sp. n., a whipworm from Octodon degus in Chile. Journal of Parasitology 61(6), 198–206.CrossRefGoogle Scholar
Babero, BB, Cattan, PE and Cabello, C (1976) A new species of whipworm from the rodent Akodon longipilis in Chile. Transactions of the American Microscopical Society 95(2), 232–235.CrossRefGoogle ScholarPubMed
Barker, FD (1915) Parasites of the American muskrat (Fiber zibethicus). Journal of Parasitology 1(4), 184–197.CrossRefGoogle Scholar
Barus, V, Madjumdar, G and Mikailov, TK (1975) Morphology and taxonomy of Trichocephalus myocastoris (Enigk, 1933). Folia Parasitologica 22(3), 207–213.Google Scholar
Boren, JC, Lochmiller, RL, Boggs, JE and Leslie, DM (1993) Gastrointestinal helminths of eastern woodrat populations in Central Oklahoma. Southwestern Naturalist 38(2), 146–149.CrossRefGoogle Scholar
Bush, A, Lafferty, KD, Lotz, JM and Shostak, W (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83(4), 575–583.CrossRefGoogle Scholar
Callejón, R, De Rojas, M, Nieberding, C, Foronda, P, Feliú, C, Guevara, D and Cutillas, C (2010) Molecular evolution of Trichuris muris isolated from different Muridae hosts in Europe. Parasitology Research 107(3), 631–641.CrossRefGoogle ScholarPubMed
Callejón, R, Nadler, S, De Rojas, M, Zurita, A, Petrášová, J and Cutillas, C (2013) Molecular characterization and phylogeny of whipworm nematodes inferred from DNA sequences of cox1 mtDNA and 18S rDNA. Parasitology Research 112(11), 3933–3949.CrossRefGoogle ScholarPubMed
Callejón, R, Robles, MR, Panei, CJ and Cutillas, C (2016) Molecular diversification of Trichuris spp. from Sigmodontinae (Cricetidae) rodents from Argentina based on mitochondrial DNA sequences. Parasitology Research 115(8), 2933–2945.CrossRefGoogle ScholarPubMed
Cameron, TWM and Reesal, MR (1951) Studies on the endoparasitic fauna of Trinidad mammals. Canadian Journal of Zoology 29(4), 276–289.CrossRefGoogle Scholar
Chandler, AC (1945) Trichuris species from California rodents. Journal of Parasitology 31(4), 284–287.CrossRefGoogle Scholar
Chandler, AC (1946) Trichuris peromysci n. sp. from Peromyscus califormcus, and further notes on T. perognathi Chandler, 1945. Journal of Parasitology 32(1), 208.CrossRefGoogle Scholar
Correa-Gomes, D, Lanfredi, RM, Pinto, RM and De Souza, W (1992) Description of Trichuris travassosi n. sp. (Nematoda: Trichurinae) from a Brazilian rodent, by light and scanning electron microscopy. Memórias do Instituto Oswaldo Cruz 87(Suppl 1), 1–10.CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9(8), 772.CrossRefGoogle ScholarPubMed
Eberhardt, AT, Robles, MR, Monje, LD, Beldomenico, PM and Callejón, R (2019) A new Trichuris species (Nematoda: Trichuridae) from capybaras: morphological–molecular characterization and phylogenetic relationships. Acta Tropica 190(1), 244–252.CrossRefGoogle ScholarPubMed
Falcón-Ordaz, J, Monzalvo-López, RJ and García-Prieto, L (2020) New species of Trichuris (Nematoda: Trichuridae) parasitizing Heteromys salvini (Rodentia: Heteromyidae) from Costa Rica, with a key to Trichuris species described from Heteromyidae. Revista Brasileira de Parasitologia Veterinária 29(2), e022019.CrossRefGoogle ScholarPubMed
Fataliev, G (1983) Trichocephalus (Trichuris) species of commercial fur-bearing animals in the Small Caucasus and the adjoining Mil-sko-Karabakhsk steppe of the Azerbaijan SSR and their ecological characteristics. Izvestiya Akademii Nauk Azerbaidzhanskoi SSR Biologicheskie Nauki 3(1), 57–61.Google Scholar
Feliu, C, Mas-Coma, S and Gallego, J (1980) Contribución al conocimiento de la helmintofauna de micromamíferos ibéricos. VII. Parásitos de Mus musculus Linnaeus, 1758 y Mus spretus Lataste, 1883 (Rodentia: Muridae) [Contribution to the knowledge of the helminthofauna of Iberian small mammals. VII. Parasites of Mus musculus Linnaeus, 1758 and Mus spretus Lataste, 1883 (Rodentia: Muridae)]. Journal of Agriculture and Rural Development in the Tropics and Subtropics 38(2), 295–309. [In Spanish.]Google Scholar
Feliu, C, Spakulová, M, Casanova, JC, Renaud, F, Morand, S, Hugot, JP, Santalla, F and Durand, P (2000) Genetic and morphological heterogeneity in small rodent whipworms in southwestern Europe: characterization of Trichuris muris and description of Trichuris arvicolae n. sp. (Nematoda: Trichuridae). Journal of Parasitology 86(3), 442–449.CrossRefGoogle Scholar
Frandsen, JC and Grundmann, AW (1961) Trichuris stansburyi and Gongylonema mysciphilia, two new species of nematodes from the deer mouse in Utah. Proceedings of the Helminthological Society of Washington 28(1), 91–94.Google Scholar
Gasser, RB, Chilton, NB, Hoste, H and Beveridge, I (1993) Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Research 21(10), 2525–2526.CrossRefGoogle ScholarPubMed
Genov, T (1984) Helminths of insectivorous mammals and rodents in Bulgaria. Sofia, Publication House of the Bulgarian Academy of Sciences.Google Scholar
Gómez Muñoz, MA, Robles, MR, Milano, AMF and Navone, GT (2018) Helminth infection levels on Rattus rattus (Rodentia: Muridae) from Corrientes city, Argentina. Mastozoología Neotropical 25(1), 221–227.CrossRefGoogle Scholar
Hall, MC (1916) Nematode parasites of mammals of the orders Rodentia, Lagomorpha, and Hyracoidea. Proceedings of the United States National Museum 50(2131), 1–258.CrossRefGoogle Scholar
Hurst, RJ and Else, KJ (2013) Trichuris muris research revisited: a journey through time. Parasitology 140(11), 1325–1339.CrossRefGoogle ScholarPubMed
Ibrahim, MA, Ogunsusi, RA, Nwude, N and Aliu, Y (1984) Helminths of the African giant rat (Cricetomys gambianus Waterhouse) in Zaria, Nigeria. Revue d’Élevage et de Médecine Vétérinaire des pays Tropicaux 37(3), 304–307.Google 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(6), 1547–1549.CrossRefGoogle ScholarPubMed
Mafiana, CF, Osho, MB and Sam-Wobo, S (1997) Gastrointestinal helminth parasites of the black rat (Rattus rattus) in Abeokuta, southwest Nigeria. Journal of Helminthology 71(3), 217–220.CrossRefGoogle ScholarPubMed
Morini, EG, Boero, J and Rodriguez, A (1955) Parásitos intestinales en el ‘Marra’ (Dolichotis patagonum patagonum) [Intestinal parasites in the ‘Marra (Dolichotis patagonum patagonum). Publicación Mision de Estudios de Patología Regional 26(1), 83–89. [In Spanish.]Google Scholar
Panti-May, JA and Robles, MR (2016) A new species of Trichuris Roederer, 1761 (Nematoda: Trichuridae) from Heteromys gaumeri Allen and Chapman (Rodentia: Heteromyidae) in Yucatan, Mexico. Systematic Parasitology 93(7), 721–730.CrossRefGoogle Scholar
Panti-May, JA, Duarte-Jiménez, A, Hernández-Betancourt, SF and Rodríguez-Vivas, RI (2021) A checklist of the helminth parasites of invasive murid rodents in Mexico. Therya 12(1), 85–93.CrossRefGoogle Scholar
Pfaffenberger, GS and Best, T (1989) Trichuris elatoris sp. n. (Nematoda: Trichuridae) from the Texas kangaroo rat (Dipodomys elator). Proceedings of the Helminthological Society of Washington 56(1), 76–81.Google Scholar
Preisser, WC and Falcon-Ordaz, J (2019) A checklist of the parasitic helminths of cricetid and heteromyid rodents in Mexico. Therya 10(3), 329–334.CrossRefGoogle Scholar
Prokopic, J and Genov, T (1984) Distribution of helminths in micro-mammals (Insectivora and Rodentia) under different ecological and geographical conditions. Academia Praha 9(1), 1–159.Google Scholar
Read, CP (1956) Trichuris dipodomis n. sp., from Ord's kangaroo rat. Proceedings of the Helminthological Society of Washington 23(1), 119.Google Scholar
Ribas, A, Wells, K, Morand, S, Chaisiri, K, Agatsuma, T, Lakim, MB, Yuh Tuh, FY and Saijuntha, W (2020) Whipworms of south-east Asian rodents are distinct from Trichuris muris. Parasitology International 77(1), 102–128.CrossRefGoogle ScholarPubMed
Robles, MR (2011) New species of Trichuris (Nematoda: Trichuridae) from Akodon montensis Thomas, 1913 of the Paranaense forest in Argentina. Journal of Parasitology 97(2), 319–327.CrossRefGoogle ScholarPubMed
Robles, MR, Navone, GT and Notarnicola, J (2006) A new species of Trichuris (Nematoda: Trichuridae) from Phyllotini Rodents in Argentina. Journal of Parasitology 92(1), 100–104.CrossRefGoogle ScholarPubMed
Robles, MR, Cutillas, C, Panei, CJ and Callejón, R (2014) Morphological and molecular characterization of a new Trichuris species (Nematoda-Trichuridae), and phylogenetic relationships of Trichuris species of cricetid rodents from Argentina. PLoS One 9(11), e112069.CrossRefGoogle ScholarPubMed
Robles, MR, Cutillas, C and Callejón, R (2018) Morphological–molecular characterization and phylogenetic relationships of a new Trichuris species (Nematoda: Trichuridae) parasitic on Holochilus chacarius (Cricetidae: Sigmodontinae) from the Chaco ecoregion (Argentina). Infection, Genetics and Evolution 58(1), 66–76.CrossRefGoogle ScholarPubMed
Roman, E (1951) Etude écologique et morphologique sur les Acanthocéphales et les Nématodes parasites des rats de la région Lyonnaise [Ecological and morphological study on Acanthocephala and parasitic Nematodes of rats in the Lyon region]. Mémoires du Muséum National d'Histoire Naturelle Série A Zoologie 2(2), 49–270. [In French.]Google Scholar
Ronquist, F and Huelsenbeck, JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12), 1572–1574.CrossRefGoogle ScholarPubMed
Schrank, FP (1788) Verzeichniß der bisher hinlänglich bekannten Eingeweidewürmer, nebst einer Abhandlung über ihre Anverwandtschaften, pp. [1–12], 1–116, 1 Tabelle. München. (Strobl). [In German.].Google Scholar
Skryabin, KI, Shikhobalova, NP and Orlov, YV (1957) Trichocephalidae and Capillariidae of animals and man and the diseases caused by them. Osnovy Nematodologii 6(1), 496. [In Russian.]Google Scholar
Smales, LR (2016) The gastrointestinal helminths of Rattus niobe (Rodentia: Muridae) with descriptions of two new genera and three new species (Nematoda) from Papua New Guinea and Papua Indonesia. Zootaxa 4117(2), 183–197.CrossRefGoogle ScholarPubMed
Suriano, DM and Navone, GT (1994) Three new species of the genus Trichuris Roederer, 1761 (Nematoda: Trichuridae) from Caviomorph and Cricetid rodents in Argentina. Research and Reviews in Parasitology 54(1), 39–46.Google Scholar
Thompson, JD, Higgins, DG and Gibson, TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22(22), 4673–4680.CrossRefGoogle ScholarPubMed
Tiner, JD (1950) Two new species of Trichuris from North America with description of Trichuris leporis (Nematoda: Aphasmidia). Journal of Parasitology 36(4), 350–354.CrossRefGoogle Scholar
Todd, SK and Lepp, LD (1972) Redescription of Trichuris fossor Hall, 1916 (Nematoda: Trichuridae) from the Northen Pocket Gopher, Thonomys talpoides. Proceedings of the Helminthological Society of Washington 39(2), 203–205.Google Scholar
Tomasovicova, O, Corba, J, Spaldonova, R and Bondy, R (1988) The susceptibility of different inbred strains of mice to Trichocephalus muris infection. Helminthologia 25(1), 273–277.Google Scholar
Torres, EJL, Nascimento, APF, Menezes, AO, Garcia, J, dos Santos, MAJ, Maldonado, A, Miranda, K, Lanfredi, RM and de Souza, W (2011) A new species of Trichuris from Thrichomys apereoides (Rodentia: Echimyidae) in Brazil: Morphological and histological studies. Veterinary Parasitology 176(2–3), 226–235.CrossRefGoogle ScholarPubMed
Wakelin, D (1994) Genetic control of immunity to helminths infections. pp. 335–359. In Chowdbury, N and Tada, IJ (Eds) Helminthology. Berlin, Springer-Verlag.CrossRefGoogle Scholar
Wasimuddin, JB, Ribas, A, Baird, SJE, Piálek, J and De Bellocq, JG (2016) Testing parasite ‘intimacy’: The whipworm Trichuris muris in the European house mouse hybrid zone. Ecology and Evolution 6(9), 2688–2701.CrossRefGoogle ScholarPubMed
Yamaguti, S (1961) Systema helminthum: Volume II. New York, Interscience Publishers Inc.Google Scholar
Zhu, XQ, Jacobs, DE, Chilton, NB, Sani, RA, Cheng, NABY and Gasser, RB (1998) Molecular characterization of a Toxocara variant from cats in Kuala Lumpur, Malaysia. Parasitology 117(2), 155–164.CrossRefGoogle ScholarPubMed
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