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Metabarcoding in two isolated populations of wild roe deer (Capreolus capreolus) reveals variation in gastrointestinal nematode community composition between regions and among age classes

BACKGROUND: Gastrointestinal nematodes are ubiquitous for both domestic and wild ungulates and have varying consequences for health and fitness. They exist as complex communities of multiple co-infecting species, and we have a limited understanding of how these communities vary in different hosts, r...

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Autores principales: Beaumelle, Camille, Redman, Elizabeth M., de Rijke, Jill, Wit, Janneke, Benabed, Slimania, Debias, François, Duhayer, Jeanne, Pardonnet, Sylvia, Poirel, Marie-Thérèse, Capron, Gilles, Chabot, Stéphane, Rey, Benjamin, Yannic, Glenn, Gilleard, John S., Bourgoin, Gilles
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8642965/
https://www.ncbi.nlm.nih.gov/pubmed/34863264
http://dx.doi.org/10.1186/s13071-021-05087-5
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author Beaumelle, Camille
Redman, Elizabeth M.
de Rijke, Jill
Wit, Janneke
Benabed, Slimania
Debias, François
Duhayer, Jeanne
Pardonnet, Sylvia
Poirel, Marie-Thérèse
Capron, Gilles
Chabot, Stéphane
Rey, Benjamin
Yannic, Glenn
Gilleard, John S.
Bourgoin, Gilles
author_facet Beaumelle, Camille
Redman, Elizabeth M.
de Rijke, Jill
Wit, Janneke
Benabed, Slimania
Debias, François
Duhayer, Jeanne
Pardonnet, Sylvia
Poirel, Marie-Thérèse
Capron, Gilles
Chabot, Stéphane
Rey, Benjamin
Yannic, Glenn
Gilleard, John S.
Bourgoin, Gilles
author_sort Beaumelle, Camille
collection PubMed
description BACKGROUND: Gastrointestinal nematodes are ubiquitous for both domestic and wild ungulates and have varying consequences for health and fitness. They exist as complex communities of multiple co-infecting species, and we have a limited understanding of how these communities vary in different hosts, regions and circumstances or of how this affects their impacts. METHODS: We have undertaken ITS2 rDNA nemabiome metabarcoding with next-generation sequencing on populations of nematode larvae isolated from 149 fecal samples of roe deer of different sex and age classes in the two isolated populations of Chizé and Trois Fontaines in France not co-grazing with any domestic ungulate species. RESULTS: We identified 100 amplified sequence variants (ASVs) that were assigned to 14 gastrointestinal nematode taxa overall at either genus (29%) or species (71%) level. These taxa were dominated by parasites classically found in cervids—e.g. Ostertagia leptospicularis, Spiculopteragia spp. Higher parasite species diversity was present in the Trois Fontaines population than in the Chizé population including the presence of species more typically seen in domestic livestock (Haemonchus contortus, Bunostomum sp., Cooperia punctata, Teladorsagia circumcincta). No differences in parasite species diversity or community composition were seen in the samples collected from three zones of differing habitat quality within the Chizé study area. Young roe deer hosted the highest diversity of gastrointestinal nematodes, with more pronounced effects of age apparent in Trois Fontaines. The effect of host age differed between gastrointestinal nematode species, e.g. there was little effect on O. leptospicularis but a large effect on Trichostrongylus spp. No effect of host sex was detected in either site. CONCLUSIONS: The presence of some livestock parasite species in the Trois Fontaines roe deer population was unexpected given the isolation of this population away from grazing domestic livestock since decades. Overall, our results illustrate the influence of host traits and the local environment on roe deer nemabiome and demonstrate the power of the nemabiome metabarcoding approach to elucidate the composition of gastrointestinal nematode communities in wildlife. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-021-05087-5.
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spelling pubmed-86429652021-12-06 Metabarcoding in two isolated populations of wild roe deer (Capreolus capreolus) reveals variation in gastrointestinal nematode community composition between regions and among age classes Beaumelle, Camille Redman, Elizabeth M. de Rijke, Jill Wit, Janneke Benabed, Slimania Debias, François Duhayer, Jeanne Pardonnet, Sylvia Poirel, Marie-Thérèse Capron, Gilles Chabot, Stéphane Rey, Benjamin Yannic, Glenn Gilleard, John S. Bourgoin, Gilles Parasit Vectors Research BACKGROUND: Gastrointestinal nematodes are ubiquitous for both domestic and wild ungulates and have varying consequences for health and fitness. They exist as complex communities of multiple co-infecting species, and we have a limited understanding of how these communities vary in different hosts, regions and circumstances or of how this affects their impacts. METHODS: We have undertaken ITS2 rDNA nemabiome metabarcoding with next-generation sequencing on populations of nematode larvae isolated from 149 fecal samples of roe deer of different sex and age classes in the two isolated populations of Chizé and Trois Fontaines in France not co-grazing with any domestic ungulate species. RESULTS: We identified 100 amplified sequence variants (ASVs) that were assigned to 14 gastrointestinal nematode taxa overall at either genus (29%) or species (71%) level. These taxa were dominated by parasites classically found in cervids—e.g. Ostertagia leptospicularis, Spiculopteragia spp. Higher parasite species diversity was present in the Trois Fontaines population than in the Chizé population including the presence of species more typically seen in domestic livestock (Haemonchus contortus, Bunostomum sp., Cooperia punctata, Teladorsagia circumcincta). No differences in parasite species diversity or community composition were seen in the samples collected from three zones of differing habitat quality within the Chizé study area. Young roe deer hosted the highest diversity of gastrointestinal nematodes, with more pronounced effects of age apparent in Trois Fontaines. The effect of host age differed between gastrointestinal nematode species, e.g. there was little effect on O. leptospicularis but a large effect on Trichostrongylus spp. No effect of host sex was detected in either site. CONCLUSIONS: The presence of some livestock parasite species in the Trois Fontaines roe deer population was unexpected given the isolation of this population away from grazing domestic livestock since decades. Overall, our results illustrate the influence of host traits and the local environment on roe deer nemabiome and demonstrate the power of the nemabiome metabarcoding approach to elucidate the composition of gastrointestinal nematode communities in wildlife. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-021-05087-5. BioMed Central 2021-12-04 /pmc/articles/PMC8642965/ /pubmed/34863264 http://dx.doi.org/10.1186/s13071-021-05087-5 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Beaumelle, Camille
Redman, Elizabeth M.
de Rijke, Jill
Wit, Janneke
Benabed, Slimania
Debias, François
Duhayer, Jeanne
Pardonnet, Sylvia
Poirel, Marie-Thérèse
Capron, Gilles
Chabot, Stéphane
Rey, Benjamin
Yannic, Glenn
Gilleard, John S.
Bourgoin, Gilles
Metabarcoding in two isolated populations of wild roe deer (Capreolus capreolus) reveals variation in gastrointestinal nematode community composition between regions and among age classes
title Metabarcoding in two isolated populations of wild roe deer (Capreolus capreolus) reveals variation in gastrointestinal nematode community composition between regions and among age classes
title_full Metabarcoding in two isolated populations of wild roe deer (Capreolus capreolus) reveals variation in gastrointestinal nematode community composition between regions and among age classes
title_fullStr Metabarcoding in two isolated populations of wild roe deer (Capreolus capreolus) reveals variation in gastrointestinal nematode community composition between regions and among age classes
title_full_unstemmed Metabarcoding in two isolated populations of wild roe deer (Capreolus capreolus) reveals variation in gastrointestinal nematode community composition between regions and among age classes
title_short Metabarcoding in two isolated populations of wild roe deer (Capreolus capreolus) reveals variation in gastrointestinal nematode community composition between regions and among age classes
title_sort metabarcoding in two isolated populations of wild roe deer (capreolus capreolus) reveals variation in gastrointestinal nematode community composition between regions and among age classes
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8642965/
https://www.ncbi.nlm.nih.gov/pubmed/34863264
http://dx.doi.org/10.1186/s13071-021-05087-5
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