Fecal microbiomes of non-human primates in Western Uganda reveal species-specific communities largely resistant to habitat perturbation

Primate gastrointestinal microbial communities are becoming increasingly appreciated for their relevance to comparative medicine and conservation, but the factors that structure primate “microbiomes” remain controversial. This study examined a community of primates in Kibale National Park, Uganda, t...

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Published inAmerican journal of primatology Vol. 76; no. 4; pp. 347 - 354
Main Authors McCord, Aleia I., Chapman, Colin A., Weny, Geoffrey, Tumukunde, Alex, Hyeroba, David, Klotz, Kelly, Koblings, Avery S., Mbora, David N.M., Cregger, Melissa, White, Bryan A., Leigh, Steven R., Goldberg, Tony L.
Format Journal Article
LanguageEnglish
Published United States Blackwell Publishing Ltd 01.04.2014
Wiley Subscription Services, Inc
Subjects
Animals
Cattle - microbiology
Cercopithecinae
Cercopithecus - microbiology
Colobinae
Colobus - microbiology
DNA, Bacterial
Domestic animals
Ecosystem
Feces - microbiology
forest fragmentation
Forests
Goats - microbiology
Humans - microbiology
Kenya
Livestock
Microbial activity
microbiome
Microbiota - genetics
National parks
non-human primate
Old World monkeys
Phylogeny
Physiology
Primates
Sheep - microbiology
Swine - microbiology
Trees
Uganda
Uganda
Colobinae
Uganda
non-human primate
Cercopithecinae
forest fragmentation
microbiome
Online AccessGet full text

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Abstract Primate gastrointestinal microbial communities are becoming increasingly appreciated for their relevance to comparative medicine and conservation, but the factors that structure primate “microbiomes” remain controversial. This study examined a community of primates in Kibale National Park, Uganda, to assess the relative importance of host species and location in structuring gastrointestinal microbiomes. Fecal samples were collected from primates in intact forest and from primates in highly disturbed forest fragments. People and livestock living nearby were also included, as was a geographically distant population of related red colobus in Kenya. A culture‐free microbial community fingerprinting technique was used to analyze fecal microbiomes from 124 individual red colobus (Procolobus rufomitratus), 100 individual black‐and‐white colobus (Colobus guereza), 111 individual red‐tailed guenons (Cercopithecus ascanius), 578 human volunteers, and 364 domestic animals, including cattle (Bos indicus and B. indicus × B. taurus crosses), goats (Caprus hircus), sheep (Ovis aries), and pigs (Sus scrofa). Microbiomes sorted strongly by host species, and forest fragmentation did not alter this pattern. Microbiomes of Kenyan red colobus sorted distinctly from microbiomes of Ugandan red colobus, but microbiomes from these two red colobus populations clustered more closely with each other than with any other species. Microbiomes from red colobus and black‐and‐white colobus were more differentiated than would be predicted by the phylogenetic relatedness of these two species, perhaps reflecting heretofore underappreciated differences in digestive physiology between the species. Within Kibale, social group membership influenced intra‐specific variation among microbiomes. However, intra‐specific variation was higher among primates in forest fragments than among primates in intact forest, perhaps reflecting the physical separation of fragments. These results suggest that, in this system, species‐specific processes such as gastrointestinal physiology strongly structure microbial communities, and that primate microbiomes are relatively resistant to perturbation, even across large geographic distances or in the face of habitat disturbance. Am. J. Primatol. 76:347–354, 2014. © 2013 Wiley Periodicals, Inc.
AbstractList Primate gastrointestinal microbial communities are becoming increasingly appreciated for their relevance to comparative medicine and conservation, but the factors that structure primate "microbiomes" remain controversial. This study examined a community of primates in Kibale National Park, Uganda, to assess the relative importance of host species and location in structuring gastrointestinal microbiomes. Fecal samples were collected from primates in intact forest and from primates in highly disturbed forest fragments. People and livestock living nearby were also included, as was a geographically distant population of related red colobus in Kenya. A culture-free microbial community fingerprinting technique was used to analyze fecal microbiomes from 124 individual red colobus (Procolobus rufomitratus), 100 individual black-and-white colobus (Colobus guereza), 111 individual red-tailed guenons (Cercopithecus ascanius), 578 human volunteers, and 364 domestic animals, including cattle (Bos indicus and B. indicus × B. taurus crosses), goats (Caprus hircus), sheep (Ovis aries), and pigs (Sus scrofa). Microbiomes sorted strongly by host species, and forest fragmentation did not alter this pattern. Microbiomes of Kenyan red colobus sorted distinctly from microbiomes of Ugandan red colobus, but microbiomes from these two red colobus populations clustered more closely with each other than with any other species. Microbiomes from red colobus and black-and-white colobus were more differentiated than would be predicted by the phylogenetic relatedness of these two species, perhaps reflecting heretofore underappreciated differences in digestive physiology between the species. Within Kibale, social group membership influenced intra-specific variation among microbiomes. However, intra-specific variation was higher among primates in forest fragments than among primates in intact forest, perhaps reflecting the physical separation of fragments. These results suggest that, in this system, species-specific processes such as gastrointestinal physiology strongly structure microbial communities, and that primate microbiomes are relatively resistant to perturbation, even across large geographic distances or in the face of habitat disturbance.
Primate gastrointestinal microbial communities are becoming increasingly appreciated for their relevance to comparative medicine and conservation, but the factors that structure primate "microbiomes" remain controversial. This study examined a community of primates in Kibale National Park, Uganda, to assess the relative importance of host species and location in structuring gastrointestinal microbiomes. Fecal samples were collected from primates in intact forest and from primates in highly disturbed forest fragments. People and livestock living nearby were also included, as was a geographically distant population of related red colobus in Kenya. A culture-free microbial community fingerprinting technique was used to analyze fecal microbiomes from 124 individual red colobus (Procolobus rufomitratus), 100 individual black-and-white colobus (Colobus guereza), 111 individual red-tailed guenons (Cercopithecus ascanius), 578 human volunteers, and 364 domestic animals, including cattle (Bos indicus and B. indicus×B. taurus crosses), goats (Caprus hircus), sheep (Ovis aries), and pigs (Sus scrofa). Microbiomes sorted strongly by host species, and forest fragmentation did not alter this pattern. Microbiomes of Kenyan red colobus sorted distinctly from microbiomes of Ugandan red colobus, but microbiomes from these two red colobus populations clustered more closely with each other than with any other species. Microbiomes from red colobus and black-and-white colobus were more differentiated than would be predicted by the phylogenetic relatedness of these two species, perhaps reflecting heretofore underappreciated differences in digestive physiology between the species. Within Kibale, social group membership influenced intra-specific variation among microbiomes. However, intra-specific variation was higher among primates in forest fragments than among primates in intact forest, perhaps reflecting the physical separation of fragments. These results suggest that, in this system, species-specific processes such as gastrointestinal physiology strongly structure microbial communities, and that primate microbiomes are relatively resistant to perturbation, even across large geographic distances or in the face of habitat disturbance. Am. J. Primatol. 76:347-354, 2014. © 2013 Wiley Periodicals, Inc. [PUBLICATION ABSTRACT]
Primate gastrointestinal microbial communities are becoming increasingly appreciated for their relevance to comparative medicine and conservation, but the factors that structure primate 'microbiomes' remain controversial. This study examined a community of primates in Kibale National Park, Uganda, to assess the relative importance of host species and location in structuring gastrointestinal microbiomes. Fecal samples were collected from primates in intact forest and from primates in highly disturbed forest fragments. People and livestock living nearby were also included, as was a geographically distant population of related red colobus in Kenya. A culture-free microbial community fingerprinting technique was used to analyze fecal microbiomes from 124 individual red colobus (Procolobus rufomitratus), 100 individual black-and-white colobus (Colobus guereza), 111 individual red-tailed guenons (Cercopithecus ascanius), 578 human volunteers, and 364 domestic animals, including cattle (Bos indicus and B. indicus B. taurus crosses), goats (Caprus hircus), sheep (Ovis aries), and pigs (Sus scrofa). Microbiomes sorted strongly by host species, and forest fragmentation did not alter this pattern. Microbiomes of Kenyan red colobus sorted distinctly from microbiomes of Ugandan red colobus, but microbiomes from these two red colobus populations clustered more closely with each other than with any other species. Microbiomes from red colobus and black-and-white colobus were more differentiated than would be predicted by the phylogenetic relatedness of these two species, perhaps reflecting heretofore underappreciated differences in digestive physiology between the species. Within Kibale, social group membership influenced intra-specific variation among microbiomes. However, intra-specific variation was higher among primates in forest fragments than among primates in intact forest, perhaps reflecting the physical separation of fragments. These results suggest that, in this system, species-specific processes such as gastrointestinal physiology strongly structure microbial communities, and that primate microbiomes are relatively resistant to perturbation, even across large geographic distances or in the face of habitat disturbance. Am. J. Primatol. 76:347-354, 2014. © 2013 Wiley Periodicals, Inc. Copyright John Wiley & Sons. Reproduced with permission. An electronic version of this article is available online at http://www.interscience.wiley.com
Primate gastrointestinal microbial communities are becoming increasingly appreciated for their relevance to comparative medicine and conservation, but the factors that structure primate “microbiomes” remain controversial. This study examined a community of primates in Kibale National Park, Uganda, to assess the relative importance of host species and location in structuring gastrointestinal microbiomes. Fecal samples were collected from primates in intact forest and from primates in highly disturbed forest fragments. People and livestock living nearby were also included, as was a geographically distant population of related red colobus in Kenya. A culture‐free microbial community fingerprinting technique was used to analyze fecal microbiomes from 124 individual red colobus ( Procolobus rufomitratus ), 100 individual black‐and‐white colobus ( Colobus guereza ), 111 individual red‐tailed guenons ( Cercopithecus ascanius ), 578 human volunteers, and 364 domestic animals, including cattle ( Bos indicus and B. indicus  ×  B. taurus crosses), goats ( Caprus hircus ), sheep ( Ovis aries ), and pigs ( Sus scrofa ). Microbiomes sorted strongly by host species, and forest fragmentation did not alter this pattern. Microbiomes of Kenyan red colobus sorted distinctly from microbiomes of Ugandan red colobus, but microbiomes from these two red colobus populations clustered more closely with each other than with any other species. Microbiomes from red colobus and black‐and‐white colobus were more differentiated than would be predicted by the phylogenetic relatedness of these two species, perhaps reflecting heretofore underappreciated differences in digestive physiology between the species. Within Kibale, social group membership influenced intra‐specific variation among microbiomes. However, intra‐specific variation was higher among primates in forest fragments than among primates in intact forest, perhaps reflecting the physical separation of fragments. These results suggest that, in this system, species‐specific processes such as gastrointestinal physiology strongly structure microbial communities, and that primate microbiomes are relatively resistant to perturbation, even across large geographic distances or in the face of habitat disturbance. Am. J. Primatol. 76:347–354, 2014. © 2013 Wiley Periodicals, Inc.
Primate gastrointestinal microbial communities are becoming increasingly appreciated for their relevance to comparative medicine and conservation, but the factors that structure primate “microbiomes” remain controversial. This study examined a community of primates in Kibale National Park, Uganda, to assess the relative importance of host species and location in structuring gastrointestinal microbiomes. Fecal samples were collected from primates in intact forest and from primates in highly disturbed forest fragments. People and livestock living nearby were also included, as was a geographically distant population of related red colobus in Kenya. A culture‐free microbial community fingerprinting technique was used to analyze fecal microbiomes from 124 individual red colobus (Procolobus rufomitratus), 100 individual black‐and‐white colobus (Colobus guereza), 111 individual red‐tailed guenons (Cercopithecus ascanius), 578 human volunteers, and 364 domestic animals, including cattle (Bos indicus and B. indicus × B. taurus crosses), goats (Caprus hircus), sheep (Ovis aries), and pigs (Sus scrofa). Microbiomes sorted strongly by host species, and forest fragmentation did not alter this pattern. Microbiomes of Kenyan red colobus sorted distinctly from microbiomes of Ugandan red colobus, but microbiomes from these two red colobus populations clustered more closely with each other than with any other species. Microbiomes from red colobus and black‐and‐white colobus were more differentiated than would be predicted by the phylogenetic relatedness of these two species, perhaps reflecting heretofore underappreciated differences in digestive physiology between the species. Within Kibale, social group membership influenced intra‐specific variation among microbiomes. However, intra‐specific variation was higher among primates in forest fragments than among primates in intact forest, perhaps reflecting the physical separation of fragments. These results suggest that, in this system, species‐specific processes such as gastrointestinal physiology strongly structure microbial communities, and that primate microbiomes are relatively resistant to perturbation, even across large geographic distances or in the face of habitat disturbance. Am. J. Primatol. 76:347–354, 2014. © 2013 Wiley Periodicals, Inc.
Primate gastrointestinal microbial communities are becoming increasingly appreciated for their relevance to comparative medicine and conservation, but the factors that structure primate “microbiomes” remain controversial. This study examined a community of primates in Kibale National Park, Uganda, to assess the relative importance of host species and location in structuring gastrointestinal microbiomes. Fecal samples were collected from primates in intact forest and from primates in highly disturbed forest fragments. People and livestock living nearby were also included, as was a geographically distant population of related red colobus in Kenya. A culture-free microbial community fingerprinting technique was used to analyze fecal microbiomes from 124 individual red colobus ( Procolobus rufomitratus ), 100 individual black-and-white colobus ( Colobus guereza ), 111 individual red-tailed guenons ( Cercopithecus ascanius ), 578 human volunteers, and 364 domestic animals, including cattle ( Bos indicus and B. indicus × B. taurus crosses ), goats ( Caprus hircus ), sheep ( Ovis aries ), and pigs ( Sus scrofa ). Microbiomes sorted strongly by host species, and forest fragmentation did not alter this pattern. Microbiomes of Kenyan red colobus sorted distinctly from microbiomes of Ugandan red colobus, but microbiomes from these two red colobus populations clustered more closely with each other than with any other species. Microbiomes from red colobus and black-and-white colobus were more differentiated than would be predicted by the phylogenetic relatedness of these two species, perhaps reflecting heretofore underappreciated differences in digestive physiology between the species. Within Kibale, social group membership influenced intra-specific variation among microbiomes. However, intra-specific variation was higher among primates in forest fragments than among primates in intact forest, perhaps reflecting the physical separation of fragments. These results suggest that, in this system, species-specific processes such as gastrointestinal physiology strongly structure microbial communities, and that primate microbiomes are relatively resistant to perturbation, even across large geographic distances or in the face of habitat disturbance.
Author Koblings, Avery S.
Hyeroba, David
White, Bryan A.
McCord, Aleia I.
Chapman, Colin A.
Mbora, David N.M.
Goldberg, Tony L.
Tumukunde, Alex
Klotz, Kelly
Cregger, Melissa
Leigh, Steven R.
Weny, Geoffrey
AuthorAffiliation 1 Nelson Institute for Environmental Studies, University of Wisconsin-Madison, Madison, Wisconsin
6 Department of Anthropology, University of Colorado at Boulder, Boulder, Colorado
2 Department of Anthropology and School of Environment, McGill University, Montreal, Quebec, Canada
3 Makerere University, Kampala, Uganda
7 Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, Wisconsin
5 Institute for Genomic Biology, University of Illinois, Urbana, Illinois
4 Departments of Biology and Environmental Science, Whittier College, Whittier, California
AuthorAffiliation_xml – name: 5 Institute for Genomic Biology, University of Illinois, Urbana, Illinois
– name: 7 Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, Wisconsin
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– name: 6 Department of Anthropology, University of Colorado at Boulder, Boulder, Colorado
– name: 2 Department of Anthropology and School of Environment, McGill University, Montreal, Quebec, Canada
– name: 3 Makerere University, Kampala, Uganda
– name: 4 Departments of Biology and Environmental Science, Whittier College, Whittier, California
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  organization: Makerere University, Uganda, Kampala
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  organization: Makerere University, Uganda, Kampala
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  surname: Hyeroba
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  organization: Makerere University, Uganda, Kampala
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  givenname: Kelly
  surname: Klotz
  fullname: Klotz, Kelly
  organization: Nelson Institute for Environmental Studies, University of Wisconsin-Madison, Wisconsin, Madison
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  organization: Nelson Institute for Environmental Studies, University of Wisconsin-Madison, Wisconsin, Madison
– sequence: 8
  givenname: David N.M.
  surname: Mbora
  fullname: Mbora, David N.M.
  organization: Departments of Biology and Environmental Science, Whittier College, California, Whittier
– sequence: 9
  givenname: Melissa
  surname: Cregger
  fullname: Cregger, Melissa
  organization: Institute for Genomic Biology, University of Illinois, Illinois, Urbana
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  surname: White
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  organization: Institute for Genomic Biology, University of Illinois, Illinois, Urbana
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  surname: Leigh
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  surname: Goldberg
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/24285224$$D View this record in MEDLINE/PubMed
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Issue 4
Keywords Colobinae
Uganda
non-human primate
Cercopithecinae
forest fragmentation
microbiome
Language English
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Snippet Primate gastrointestinal microbial communities are becoming increasingly appreciated for their relevance to comparative medicine and conservation, but the...
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SubjectTerms Animals
Cattle - microbiology
Cercopithecinae
Cercopithecus - microbiology
Colobinae
Colobus - microbiology
DNA, Bacterial
Domestic animals
Ecosystem
Feces - microbiology
forest fragmentation
Forests
Goats - microbiology
Humans - microbiology
Kenya
Livestock
Microbial activity
microbiome
Microbiota - genetics
National parks
non-human primate
Old World monkeys
Phylogeny
Physiology
Primates
Sheep - microbiology
Swine - microbiology
Trees
Uganda
Title Fecal microbiomes of non-human primates in Western Uganda reveal species-specific communities largely resistant to habitat perturbation
URI https://api.istex.fr/ark:/67375/WNG-60DM41SD-X/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fajp.22238
https://www.ncbi.nlm.nih.gov/pubmed/24285224
https://www.proquest.com/docview/1506478538
https://search.proquest.com/docview/1507792110
https://search.proquest.com/docview/1515984058
https://pubmed.ncbi.nlm.nih.gov/PMC4097101
Volume 76
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