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

  1. Camille Beaumelle
  2. Carole Toïgo
  3. Rodolphe Papet
  4. Slimania Benabed
  5. Mathieu Beurier
  6. Léa Bordes
  7. Anaïs Brignone
  8. Nadine Curt-Grand-Gaudin
  9. Mathieu Garel
  10. Justine Ginot
  11. Philippe Jacquiet
  12. Christian Miquel
  13. Marie-Thérèse Poirel
  14. Anna Serafino
  15. Eric Vannard
  16. Gilles Bourgoin
  17. Glenn Yannic

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Abstract

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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  1. Version published to 10.24072/pcjournal.477
  2. Peer Community In Zoology

    Gastrointestinal nematodes represent a major problem for livestock production across the globe, one that has intensified with the rapid and repeated evolution of multi-drug resistance (Wit et al., 2021). Understanding parasite exposure and how resistance is maintained over time are therefore of key importance for defining efficient management strategies. To date, the role wildlife play in these dynamics has been poorly studied. The work of Beaumelle et al. examine this essential question by studying the transmission dynamics of nematodes at the environmental interface between transhumant sheep and wild ungulates, more specifically with ibex (Capra ibex) that allochronically share alpine pastures when sheep are brought to graze in summer. By collecting fresh fecal material from both species and using a metabarcoding approach based on ITS-2 sequences, the authors characterise the nemabiome in each ungulate species and demonstrate that the two host species share a large portion of their parasite diversity. More importantly, by focusing on a gene (β-tubulin isotype 1) associated with resistance to a commonly used anthelmintic drug (benzimidazole), they demonstrate that both species carry resistant nematode strains, but that the diversity of strains, and particularly susceptible strains, is much higher in ibex. A key feature of the sampling design is that fecal material from both species was collected before seasonal transmission between the ungulate species could occur. Therefore, their results demonstrate that ibex are able to maintain resistant strains over long periods of time and therefore may be major nematode reservoirs for sheep infection. This important conclusion raises a series of key questions. How are resistant genotypes maintained in untreated ibex hosts? Is the cost of resistance so weak that they can coexist with susceptible strains in the absence of drug treatment or does anthelminthic contamination of the pastures maintain resistant genotypes directly in wild hosts? This work also opens several interesting perspectives: For example, what additional resistant parasites may be maintained by these wildlife hosts? What role do other wild ungulate species play in the evolution of nematode communities in transhumant sheep? An expansion of this work to the larger community of wild ungulates using alpine pastures, and an evaluation of the degree to which wild species are exposed to anthelminthic drugs released by grazing livestock into the environment is now required to understand the deeper consequences of drug treatment for shaping parasite communities and their cascading impacts for wildlife conservation, and the development of efficient and sustainable management strategies for pastoral livestock. 

    References

    Beaumelle et al. Cross-transmission of resistant gastrointestinal nematodes between wildlife and transhumant sheep. bioRxiv, ver. 5 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2023.07.21.550073

    Wit, J., Dilks, C.M., Andersen, E.C., 2021. Complementary Approaches with Free-living and Parasitic Nematodes to Understanding Anthelmintic Resistance. Trends Parasitol. 37, 240–250. https://doi.org/10.1016/j.pt.2020.11.008

  3. Version published to 10.1101/2023.07.21.550073 on bioRxiv