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Multilevel social structure and diet shape the gut microbiota of the gelada monkey, the only grazing primate

BACKGROUND: The gelada monkey (Theropithecus gelada), endemic to the Ethiopian highlands, is the only graminivorous primate, i.e., it feeds mainly on grasses and sedges. In spite of known dental, manual, and locomotor adaptations, the intestinal anatomy of geladas is similar to that of other primate...

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Autores principales: Trosvik, Pål, de Muinck, Eric J., Rueness, Eli K., Fashing, Peter J., Beierschmitt, Evan C., Callingham, Kadie R., Kraus, Jacob B., Trew, Thomas H., Moges, Amera, Mekonnen, Addisu, Venkataraman, Vivek V., Nguyen, Nga
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5935910/
https://www.ncbi.nlm.nih.gov/pubmed/29729671
http://dx.doi.org/10.1186/s40168-018-0468-6
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author Trosvik, Pål
de Muinck, Eric J.
Rueness, Eli K.
Fashing, Peter J.
Beierschmitt, Evan C.
Callingham, Kadie R.
Kraus, Jacob B.
Trew, Thomas H.
Moges, Amera
Mekonnen, Addisu
Venkataraman, Vivek V.
Nguyen, Nga
author_facet Trosvik, Pål
de Muinck, Eric J.
Rueness, Eli K.
Fashing, Peter J.
Beierschmitt, Evan C.
Callingham, Kadie R.
Kraus, Jacob B.
Trew, Thomas H.
Moges, Amera
Mekonnen, Addisu
Venkataraman, Vivek V.
Nguyen, Nga
author_sort Trosvik, Pål
collection PubMed
description BACKGROUND: The gelada monkey (Theropithecus gelada), endemic to the Ethiopian highlands, is the only graminivorous primate, i.e., it feeds mainly on grasses and sedges. In spite of known dental, manual, and locomotor adaptations, the intestinal anatomy of geladas is similar to that of other primates. We currently lack a clear understanding of the adaptations in digestive physiology necessary for this species to subsist on a graminoid-based diet, but digestion in other graminivores, such as ruminants, relies heavily on the microbial community residing in the gastrointestinal (GI) system. Furthermore, geladas form complex, multilevel societies, making them a suitable system for investigating links between sociality and the GI microbiota. RESULTS: Here, we explore the gastrointestinal microbiota of gelada monkeys inhabiting an intact ecosystem and document how factors like multilevel social structure and seasonal changes in diet shape the GI microbiota. We compare the gelada GI microbiota to those of other primate species, reporting a gradient from geladas to herbivorous specialist monkeys to dietary generalist monkeys and lastly humans, the ultimate ecological generalists. We also compare the microbiotas of the gelada GI tract and the sheep rumen, finding that geladas are highly enriched for cellulolytic bacteria associated with ruminant digestion, relative to other primates. CONCLUSIONS: This study represents the first analysis of the gelada GI microbiota, providing insights into the adaptations underlying graminivory in a primate. Our results also highlight the role of social organization in structuring the GI microbiota within a society of wild animals. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0468-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-59359102018-05-11 Multilevel social structure and diet shape the gut microbiota of the gelada monkey, the only grazing primate Trosvik, Pål de Muinck, Eric J. Rueness, Eli K. Fashing, Peter J. Beierschmitt, Evan C. Callingham, Kadie R. Kraus, Jacob B. Trew, Thomas H. Moges, Amera Mekonnen, Addisu Venkataraman, Vivek V. Nguyen, Nga Microbiome Research BACKGROUND: The gelada monkey (Theropithecus gelada), endemic to the Ethiopian highlands, is the only graminivorous primate, i.e., it feeds mainly on grasses and sedges. In spite of known dental, manual, and locomotor adaptations, the intestinal anatomy of geladas is similar to that of other primates. We currently lack a clear understanding of the adaptations in digestive physiology necessary for this species to subsist on a graminoid-based diet, but digestion in other graminivores, such as ruminants, relies heavily on the microbial community residing in the gastrointestinal (GI) system. Furthermore, geladas form complex, multilevel societies, making them a suitable system for investigating links between sociality and the GI microbiota. RESULTS: Here, we explore the gastrointestinal microbiota of gelada monkeys inhabiting an intact ecosystem and document how factors like multilevel social structure and seasonal changes in diet shape the GI microbiota. We compare the gelada GI microbiota to those of other primate species, reporting a gradient from geladas to herbivorous specialist monkeys to dietary generalist monkeys and lastly humans, the ultimate ecological generalists. We also compare the microbiotas of the gelada GI tract and the sheep rumen, finding that geladas are highly enriched for cellulolytic bacteria associated with ruminant digestion, relative to other primates. CONCLUSIONS: This study represents the first analysis of the gelada GI microbiota, providing insights into the adaptations underlying graminivory in a primate. Our results also highlight the role of social organization in structuring the GI microbiota within a society of wild animals. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0468-6) contains supplementary material, which is available to authorized users. BioMed Central 2018-05-05 /pmc/articles/PMC5935910/ /pubmed/29729671 http://dx.doi.org/10.1186/s40168-018-0468-6 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Trosvik, Pål
de Muinck, Eric J.
Rueness, Eli K.
Fashing, Peter J.
Beierschmitt, Evan C.
Callingham, Kadie R.
Kraus, Jacob B.
Trew, Thomas H.
Moges, Amera
Mekonnen, Addisu
Venkataraman, Vivek V.
Nguyen, Nga
Multilevel social structure and diet shape the gut microbiota of the gelada monkey, the only grazing primate
title Multilevel social structure and diet shape the gut microbiota of the gelada monkey, the only grazing primate
title_full Multilevel social structure and diet shape the gut microbiota of the gelada monkey, the only grazing primate
title_fullStr Multilevel social structure and diet shape the gut microbiota of the gelada monkey, the only grazing primate
title_full_unstemmed Multilevel social structure and diet shape the gut microbiota of the gelada monkey, the only grazing primate
title_short Multilevel social structure and diet shape the gut microbiota of the gelada monkey, the only grazing primate
title_sort multilevel social structure and diet shape the gut microbiota of the gelada monkey, the only grazing primate
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5935910/
https://www.ncbi.nlm.nih.gov/pubmed/29729671
http://dx.doi.org/10.1186/s40168-018-0468-6
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