Refugia or reservoir? Feral goats and their role in the maintenance and circulation of benzimidazole-resistant gastrointestinal nematodes on shared pastures
Gastrointestinal nematodes threaten the productivity of grazing livestock and anthelmintic resistance has emerged globally. It is broadly understood that wild ruminants living in sympatry with livestock act as a positive source of refugia for anthelmintic-susceptible nematodes. However, they might a...
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Cambridge University Press
2023-07-01
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Series: | Parasitology |
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Online Access: | https://www.cambridge.org/core/product/identifier/S0031182023000380/type/journal_article |
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author | Emily Kate Francis Jan Šlapeta |
author_facet | Emily Kate Francis Jan Šlapeta |
author_sort | Emily Kate Francis |
collection | DOAJ |
description | Gastrointestinal nematodes threaten the productivity of grazing livestock and anthelmintic resistance has emerged globally. It is broadly understood that wild ruminants living in sympatry with livestock act as a positive source of refugia for anthelmintic-susceptible nematodes. However, they might also act as reservoirs of anthelmintic-resistant nematodes, contributing to the spread of anthelmintic resistance at a regional scale. Here, we sampled managed sheep and cattle together with feral goats within the same property in New South Wales, Australia. Internal transcribed spacer 2 (ITS-2) nemabiome metabarcoding identified 12 gastrointestinal nematodes (Cooperia oncophora, Cooperia punctata, Haemonchus contortus, Haemonchus placei, Nematodirus spathiger, Ostertagia ostertagi, Teladorsagia circumcincta, Oesophagostomum radiatum, Oesophagostomum venulosum, Trichostrongylus axei, Trichostrongylus colubriformis and Trichostrongylus rugatus). Isotype-1 β-tubulin metabarcoding targeting benzimidazole resistance polymorphisms identified 6 of these nematode species (C. oncophora, C. punctata, H. contortus, H. placei, O. ostertagi and T. circumcincta), with the remaining 3 genera unable to be identified to the species level (Nematodirus, Oesophagostomum, Trichostrongylus). Both ITS-2 and β-tubulin metabarcoding showed the presence of a cryptic species of T. circumcincta, known from domestic goats in France. Of the gastrointestinal nematodes detected via β-tubulin metabarcoding, H. contortus, T. circumcincta, Nematodirus and Trichostrongylus exhibited the presence of at least one resistance genotype. We found that generalist gastrointestinal nematodes in untreated feral goats had a similarly high frequency of the benzimidazole-resistant F200Y polymorphism as those nematodes in sheep and cattle. This suggests cross-transmission and maintenance of the resistant genotype within the wild ruminant population, affirming that wild ruminants should be considered potential reservoirs of anthelmintic resistance. |
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issn | 0031-1820 1469-8161 |
language | English |
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publishDate | 2023-07-01 |
publisher | Cambridge University Press |
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series | Parasitology |
spelling | doaj.art-6247bc9d2c6146cebb4722b3d51004d32023-07-24T11:58:56ZengCambridge University PressParasitology0031-18201469-81612023-07-0115067268210.1017/S0031182023000380Refugia or reservoir? Feral goats and their role in the maintenance and circulation of benzimidazole-resistant gastrointestinal nematodes on shared pasturesEmily Kate Francis0Jan Šlapeta1https://orcid.org/0000-0003-1459-9117Sydney School of Veterinary Science, Faculty of Science, The University of Sydney, New South Wales 2006, AustraliaSydney School of Veterinary Science, Faculty of Science, The University of Sydney, New South Wales 2006, Australia The University of Sydney Institute for Infectious Diseases, New South Wales 2006, AustraliaGastrointestinal nematodes threaten the productivity of grazing livestock and anthelmintic resistance has emerged globally. It is broadly understood that wild ruminants living in sympatry with livestock act as a positive source of refugia for anthelmintic-susceptible nematodes. However, they might also act as reservoirs of anthelmintic-resistant nematodes, contributing to the spread of anthelmintic resistance at a regional scale. Here, we sampled managed sheep and cattle together with feral goats within the same property in New South Wales, Australia. Internal transcribed spacer 2 (ITS-2) nemabiome metabarcoding identified 12 gastrointestinal nematodes (Cooperia oncophora, Cooperia punctata, Haemonchus contortus, Haemonchus placei, Nematodirus spathiger, Ostertagia ostertagi, Teladorsagia circumcincta, Oesophagostomum radiatum, Oesophagostomum venulosum, Trichostrongylus axei, Trichostrongylus colubriformis and Trichostrongylus rugatus). Isotype-1 β-tubulin metabarcoding targeting benzimidazole resistance polymorphisms identified 6 of these nematode species (C. oncophora, C. punctata, H. contortus, H. placei, O. ostertagi and T. circumcincta), with the remaining 3 genera unable to be identified to the species level (Nematodirus, Oesophagostomum, Trichostrongylus). Both ITS-2 and β-tubulin metabarcoding showed the presence of a cryptic species of T. circumcincta, known from domestic goats in France. Of the gastrointestinal nematodes detected via β-tubulin metabarcoding, H. contortus, T. circumcincta, Nematodirus and Trichostrongylus exhibited the presence of at least one resistance genotype. We found that generalist gastrointestinal nematodes in untreated feral goats had a similarly high frequency of the benzimidazole-resistant F200Y polymorphism as those nematodes in sheep and cattle. This suggests cross-transmission and maintenance of the resistant genotype within the wild ruminant population, affirming that wild ruminants should be considered potential reservoirs of anthelmintic resistance.https://www.cambridge.org/core/product/identifier/S0031182023000380/type/journal_articleBenzimidazole resistancecryptic speciesisotype-1 β-tubulinITS-2 rDNAlivestocknemabiome metabarcodingTeladorsagia circumcinctawild ruminants |
spellingShingle | Emily Kate Francis Jan Šlapeta Refugia or reservoir? Feral goats and their role in the maintenance and circulation of benzimidazole-resistant gastrointestinal nematodes on shared pastures Parasitology Benzimidazole resistance cryptic species isotype-1 β-tubulin ITS-2 rDNA livestock nemabiome metabarcoding Teladorsagia circumcincta wild ruminants |
title | Refugia or reservoir? Feral goats and their role in the maintenance and circulation of benzimidazole-resistant gastrointestinal nematodes on shared pastures |
title_full | Refugia or reservoir? Feral goats and their role in the maintenance and circulation of benzimidazole-resistant gastrointestinal nematodes on shared pastures |
title_fullStr | Refugia or reservoir? Feral goats and their role in the maintenance and circulation of benzimidazole-resistant gastrointestinal nematodes on shared pastures |
title_full_unstemmed | Refugia or reservoir? Feral goats and their role in the maintenance and circulation of benzimidazole-resistant gastrointestinal nematodes on shared pastures |
title_short | Refugia or reservoir? Feral goats and their role in the maintenance and circulation of benzimidazole-resistant gastrointestinal nematodes on shared pastures |
title_sort | refugia or reservoir feral goats and their role in the maintenance and circulation of benzimidazole resistant gastrointestinal nematodes on shared pastures |
topic | Benzimidazole resistance cryptic species isotype-1 β-tubulin ITS-2 rDNA livestock nemabiome metabarcoding Teladorsagia circumcincta wild ruminants |
url | https://www.cambridge.org/core/product/identifier/S0031182023000380/type/journal_article |
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