Cross-transmission of resistant gastrointestinal nematodes between wildlife and transhumant sheep

Wild and domestic ungulates can be infected with the same species of gastrointestinal parasitic nematodes. These parasites have free-living stages in the environment that contribute to the ease of transmission among different host species. In addition, gastrointestinal nematodes have developed resis...

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Main Authors: Beaumelle, Camille, Toïgo, Carole, Papet, Rodolphe, Benabed, Slimania, Beurier, Mathieu, Bordes, Léa, Brignone, Anaïs, Curt-Grand-Gaudin, Nadine, Garel, Mathieu, Ginot, Justine, Jacquiet, Philippe, Miquel, Christian, Poirel, Marie-Thérèse, Serafino, Anna, Vannard, Eric, Bourgoin, Gilles, Yannic, Glenn
Format: Article
Language:English
Published: Peer Community In 2024-10-01
Series:Peer Community Journal
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Online Access:https://peercommunityjournal.org/articles/10.24072/pcjournal.477/
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author Beaumelle, Camille
Toïgo, Carole
Papet, Rodolphe
Benabed, Slimania
Beurier, Mathieu
Bordes, Léa
Brignone, Anaïs
Curt-Grand-Gaudin, Nadine
Garel, Mathieu
Ginot, Justine
Jacquiet, Philippe
Miquel, Christian
Poirel, Marie-Thérèse
Serafino, Anna
Vannard, Eric
Bourgoin, Gilles
Yannic, Glenn
author_facet Beaumelle, Camille
Toïgo, Carole
Papet, Rodolphe
Benabed, Slimania
Beurier, Mathieu
Bordes, Léa
Brignone, Anaïs
Curt-Grand-Gaudin, Nadine
Garel, Mathieu
Ginot, Justine
Jacquiet, Philippe
Miquel, Christian
Poirel, Marie-Thérèse
Serafino, Anna
Vannard, Eric
Bourgoin, Gilles
Yannic, Glenn
author_sort Beaumelle, Camille
collection DOAJ
description Wild and domestic ungulates can be infected with the same species of gastrointestinal parasitic nematodes. These parasites have free-living stages in the environment that contribute to the ease of transmission among different host species. In addition, gastrointestinal nematodes have developed resistance to anthelmintics which is now considered a major problem for the livestock sector. In a context where wild and domestic ungulates share the same pastures, the maintenance and circulation of resistant gastrointestinal nematodes between species have rarely been explored. In the European Alps, domestic sheep are driven to high-altitude summer pastures and live in sympatry with wild ungulates for several months each year. In this study, we investigated the nemabiome of domestic sheep and Alpine ibex, Capra ibex, in three different areas of the French Alps to evaluate parasite circulation between the two host species. The Alpine ibex is a protected mountain ungulate that is phylogenetically related to sheep and hosts nematode species common to sheep. Using internal transcribed spacer 2 (ITS-2) nemabiome metabarcoding, we found sheep and ibex share similar gastrointestinal nematodes, except for a few species such as Marshallagia marshalli and Trichostrongylus axei. This suggests that the long-term co-occurrence of sheep and ibex on mountain pastures has promoted the exchange of gastrointestinal nematodes between the two hosts. Based on the sequencing of the isotype 1 of the beta tubulin gene, associated with benzimidazole resistance, we found resistant nematodes in all sheep flocks and in all ibex populations. Our results demonstrated that ibex can host and shed resistant strains before transhumant sheep arrive on pastures, and thus could act as a refuge or even contribute to maintaining resistant gastrointestinal nematodes. The relative role of ibex in the maintenance and circulation of resistant strains in sheep remain to be determined.
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spelling doaj-art-bfebfa8d25084d20be41760dfef937e42025-02-07T10:17:17ZengPeer Community InPeer Community Journal2804-38712024-10-01410.24072/pcjournal.47710.24072/pcjournal.477Cross-transmission of resistant gastrointestinal nematodes between wildlife and transhumant sheep Beaumelle, Camille0Toïgo, Carole1Papet, Rodolphe2Benabed, Slimania3Beurier, Mathieu4Bordes, Léa5Brignone, Anaïs6Curt-Grand-Gaudin, Nadine7Garel, Mathieu8Ginot, Justine9Jacquiet, Philippe10Miquel, Christian11Poirel, Marie-Thérèse12Serafino, Anna13Vannard, Eric14Bourgoin, Gilles15Yannic, Glenn16Université de Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR 5558, Villeurbanne, France; Université de Lyon, VetAgro Sup, Campus Vétérinaire de Lyon, Marcy l’Etoile, France; Université Grenoble Alpes, Université Savoie Mont Blanc, CNRS, LECA, Grenoble, FranceOffice Français de la Biodiversité, Service Anthropisation et Fonctionnement des Ecosystèmes Terrestres, Gières, FranceParc national des Écrins, Secteur du Champsaur-Valgaudemar, Saint Jean Saint Nicolas, FranceUniversité de Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR 5558, Villeurbanne, France; Université de Lyon, VetAgro Sup, Campus Vétérinaire de Lyon, Marcy l’Etoile, FranceOffice Français de la Biodiversité, Service Anthropisation et Fonctionnement des Ecosystèmes Terrestres, Gières, FranceUniversité de Toulouse, UMT Pilotage de la Santé des Ruminants, Ecole Nationale Vétérinaire de Toulouse, FranceOffice Français de la Biodiversité, Unité Ongulés Sauvages, Gières, FranceUniversité Grenoble Alpes, Université Savoie Mont Blanc, CNRS, LECA, Grenoble, FranceOffice Français de la Biodiversité, Service Anthropisation et Fonctionnement des Ecosystèmes Terrestres, Gières, FranceUniversité de Lyon, VetAgro Sup, Campus Vétérinaire de Lyon, Marcy l’Etoile, FranceUniversité de Toulouse, UMT Pilotage de la Santé des Ruminants, Ecole Nationale Vétérinaire de Toulouse, FranceUniversité Grenoble Alpes, Université Savoie Mont Blanc, CNRS, LECA, Grenoble, FranceUniversité de Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR 5558, Villeurbanne, France; Université de Lyon, VetAgro Sup, Campus Vétérinaire de Lyon, Marcy l’Etoile, FranceUniversité de Lyon, VetAgro Sup, Campus Vétérinaire de Lyon, Marcy l’Etoile, FranceParc national des Écrins, Secteur du Briançonnais, Briançon, FranceUniversité de Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR 5558, Villeurbanne, France; Université de Lyon, VetAgro Sup, Campus Vétérinaire de Lyon, Marcy l’Etoile, FranceUniversité Grenoble Alpes, Université Savoie Mont Blanc, CNRS, LECA, Grenoble, FranceWild and domestic ungulates can be infected with the same species of gastrointestinal parasitic nematodes. These parasites have free-living stages in the environment that contribute to the ease of transmission among different host species. In addition, gastrointestinal nematodes have developed resistance to anthelmintics which is now considered a major problem for the livestock sector. In a context where wild and domestic ungulates share the same pastures, the maintenance and circulation of resistant gastrointestinal nematodes between species have rarely been explored. In the European Alps, domestic sheep are driven to high-altitude summer pastures and live in sympatry with wild ungulates for several months each year. In this study, we investigated the nemabiome of domestic sheep and Alpine ibex, Capra ibex, in three different areas of the French Alps to evaluate parasite circulation between the two host species. The Alpine ibex is a protected mountain ungulate that is phylogenetically related to sheep and hosts nematode species common to sheep. Using internal transcribed spacer 2 (ITS-2) nemabiome metabarcoding, we found sheep and ibex share similar gastrointestinal nematodes, except for a few species such as Marshallagia marshalli and Trichostrongylus axei. This suggests that the long-term co-occurrence of sheep and ibex on mountain pastures has promoted the exchange of gastrointestinal nematodes between the two hosts. Based on the sequencing of the isotype 1 of the beta tubulin gene, associated with benzimidazole resistance, we found resistant nematodes in all sheep flocks and in all ibex populations. Our results demonstrated that ibex can host and shed resistant strains before transhumant sheep arrive on pastures, and thus could act as a refuge or even contribute to maintaining resistant gastrointestinal nematodes. The relative role of ibex in the maintenance and circulation of resistant strains in sheep remain to be determined.https://peercommunityjournal.org/articles/10.24072/pcjournal.477/ITS-2 rDNA, benzimidazole resistance, β-tubulin isotype 1, livestock, nemabiome metabarcoding, wild ungulates, transhumant sheep, Alpine ibex
spellingShingle Beaumelle, Camille
Toïgo, Carole
Papet, Rodolphe
Benabed, Slimania
Beurier, Mathieu
Bordes, Léa
Brignone, Anaïs
Curt-Grand-Gaudin, Nadine
Garel, Mathieu
Ginot, Justine
Jacquiet, Philippe
Miquel, Christian
Poirel, Marie-Thérèse
Serafino, Anna
Vannard, Eric
Bourgoin, Gilles
Yannic, Glenn
Cross-transmission of resistant gastrointestinal nematodes between wildlife and transhumant sheep
Peer Community Journal
ITS-2 rDNA, benzimidazole resistance, β-tubulin isotype 1, livestock, nemabiome metabarcoding, wild ungulates, transhumant sheep, Alpine ibex
title Cross-transmission of resistant gastrointestinal nematodes between wildlife and transhumant sheep
title_full Cross-transmission of resistant gastrointestinal nematodes between wildlife and transhumant sheep
title_fullStr Cross-transmission of resistant gastrointestinal nematodes between wildlife and transhumant sheep
title_full_unstemmed Cross-transmission of resistant gastrointestinal nematodes between wildlife and transhumant sheep
title_short Cross-transmission of resistant gastrointestinal nematodes between wildlife and transhumant sheep
title_sort cross transmission of resistant gastrointestinal nematodes between wildlife and transhumant sheep
topic ITS-2 rDNA, benzimidazole resistance, β-tubulin isotype 1, livestock, nemabiome metabarcoding, wild ungulates, transhumant sheep, Alpine ibex
url https://peercommunityjournal.org/articles/10.24072/pcjournal.477/
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