Social network community structure and the contact-mediated sharing of commensal E. coli among captive rhesus macaques (Macaca mulatta)

In group-living animals, heterogeneity in individuals’ social connections may mediate the sharing of microbial infectious agents. In this regard, the genetic relatedness of individuals’ commensal gut bacterium Escherichia coli may be ideal to assess the potential for pathogen transmission through an...

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Main Authors: Krishna Balasubramaniam, Brianne Beisner, Jiahui Guan, Jessica Vandeleest, Hsieh Fushing, Edward Atwill, Brenda McCowan
Format: Article
Language:English
Published: PeerJ Inc. 2018-01-01
Series:PeerJ
Subjects:
Online Access:https://peerj.com/articles/4271.pdf
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spelling doaj-9bcdb0b17e234b65bc0f66eeba4945fd2020-11-24T22:19:30ZengPeerJ Inc.PeerJ2167-83592018-01-016e427110.7717/peerj.4271Social network community structure and the contact-mediated sharing of commensal E. coli among captive rhesus macaques (Macaca mulatta)Krishna Balasubramaniam0Brianne Beisner1Jiahui Guan2Jessica Vandeleest3Hsieh Fushing4Edward Atwill5Brenda McCowan6Department of Population Health & Reproduction, School of Veterinary Medicine, University of California, Davis, CA, United States of AmericaDepartment of Population Health & Reproduction, School of Veterinary Medicine, University of California, Davis, CA, United States of AmericaDepartment of Statistics, University of California, Davis, CA, United States of AmericaDepartment of Population Health & Reproduction, School of Veterinary Medicine, University of California, Davis, CA, United States of AmericaDepartment of Statistics, University of California, Davis, CA, United States of AmericaDepartment of Population Health & Reproduction, School of Veterinary Medicine, University of California, Davis, CA, United States of AmericaDepartment of Population Health & Reproduction, School of Veterinary Medicine, University of California, Davis, CA, United States of AmericaIn group-living animals, heterogeneity in individuals’ social connections may mediate the sharing of microbial infectious agents. In this regard, the genetic relatedness of individuals’ commensal gut bacterium Escherichia coli may be ideal to assess the potential for pathogen transmission through animal social networks. Here we use microbial phylogenetics and population genetics approaches, as well as host social network reconstruction, to assess evidence for the contact-mediated sharing of E. coli among three groups of captively housed rhesus macaques (Macaca mulatta), at multiple organizational scales. For each group, behavioral data on grooming, huddling, and aggressive interactions collected for a six-week period were used to reconstruct social network communities via the Data Cloud Geometry (DCG) clustering algorithm. Further, an E. coli isolate was biochemically confirmed and genotypically fingerprinted from fecal swabs collected from each macaque. Population genetics approaches revealed that Group Membership, in comparison to intrinsic attributes like age, sex, and/or matriline membership of individuals, accounted for the highest proportion of variance in E. coli genotypic similarity. Social network approaches revealed that such sharing was evident at the community-level rather than the dyadic level. Specifically, although we found no links between dyadic E. coli similarity and social contact frequencies, similarity was significantly greater among macaques within the same social network communities compared to those across different communities. Moreover, tests for one of our study-groups confirmed that E. coli isolated from macaque rectal swabs were more genotypically similar to each other than they were to isolates from environmentally deposited feces. In summary, our results suggest that among frequently interacting, spatially constrained macaques with complex social relationships, microbial sharing via fecal-oral, social contact-mediated routes may depend on both individuals’ direct connections and on secondary network pathways that define community structure. They lend support to the hypothesis that social network communities may act as bottlenecks to contain the spread of infectious agents, thereby encouraging disease control strategies to focus on multiple organizational scales. Future directions includeincreasing microbial sampling effort per individual to better-detect dyadic transmission events, and assessments of the co-evolutionary links between sociality, infectious agent risk, and host immune function.https://peerj.com/articles/4271.pdfSocial networksCommunity structureMicrobial sharingCommensal E. coliRhesus macaque
collection DOAJ
language English
format Article
sources DOAJ
author Krishna Balasubramaniam
Brianne Beisner
Jiahui Guan
Jessica Vandeleest
Hsieh Fushing
Edward Atwill
Brenda McCowan
spellingShingle Krishna Balasubramaniam
Brianne Beisner
Jiahui Guan
Jessica Vandeleest
Hsieh Fushing
Edward Atwill
Brenda McCowan
Social network community structure and the contact-mediated sharing of commensal E. coli among captive rhesus macaques (Macaca mulatta)
PeerJ
Social networks
Community structure
Microbial sharing
Commensal E. coli
Rhesus macaque
author_facet Krishna Balasubramaniam
Brianne Beisner
Jiahui Guan
Jessica Vandeleest
Hsieh Fushing
Edward Atwill
Brenda McCowan
author_sort Krishna Balasubramaniam
title Social network community structure and the contact-mediated sharing of commensal E. coli among captive rhesus macaques (Macaca mulatta)
title_short Social network community structure and the contact-mediated sharing of commensal E. coli among captive rhesus macaques (Macaca mulatta)
title_full Social network community structure and the contact-mediated sharing of commensal E. coli among captive rhesus macaques (Macaca mulatta)
title_fullStr Social network community structure and the contact-mediated sharing of commensal E. coli among captive rhesus macaques (Macaca mulatta)
title_full_unstemmed Social network community structure and the contact-mediated sharing of commensal E. coli among captive rhesus macaques (Macaca mulatta)
title_sort social network community structure and the contact-mediated sharing of commensal e. coli among captive rhesus macaques (macaca mulatta)
publisher PeerJ Inc.
series PeerJ
issn 2167-8359
publishDate 2018-01-01
description In group-living animals, heterogeneity in individuals’ social connections may mediate the sharing of microbial infectious agents. In this regard, the genetic relatedness of individuals’ commensal gut bacterium Escherichia coli may be ideal to assess the potential for pathogen transmission through animal social networks. Here we use microbial phylogenetics and population genetics approaches, as well as host social network reconstruction, to assess evidence for the contact-mediated sharing of E. coli among three groups of captively housed rhesus macaques (Macaca mulatta), at multiple organizational scales. For each group, behavioral data on grooming, huddling, and aggressive interactions collected for a six-week period were used to reconstruct social network communities via the Data Cloud Geometry (DCG) clustering algorithm. Further, an E. coli isolate was biochemically confirmed and genotypically fingerprinted from fecal swabs collected from each macaque. Population genetics approaches revealed that Group Membership, in comparison to intrinsic attributes like age, sex, and/or matriline membership of individuals, accounted for the highest proportion of variance in E. coli genotypic similarity. Social network approaches revealed that such sharing was evident at the community-level rather than the dyadic level. Specifically, although we found no links between dyadic E. coli similarity and social contact frequencies, similarity was significantly greater among macaques within the same social network communities compared to those across different communities. Moreover, tests for one of our study-groups confirmed that E. coli isolated from macaque rectal swabs were more genotypically similar to each other than they were to isolates from environmentally deposited feces. In summary, our results suggest that among frequently interacting, spatially constrained macaques with complex social relationships, microbial sharing via fecal-oral, social contact-mediated routes may depend on both individuals’ direct connections and on secondary network pathways that define community structure. They lend support to the hypothesis that social network communities may act as bottlenecks to contain the spread of infectious agents, thereby encouraging disease control strategies to focus on multiple organizational scales. Future directions includeincreasing microbial sampling effort per individual to better-detect dyadic transmission events, and assessments of the co-evolutionary links between sociality, infectious agent risk, and host immune function.
topic Social networks
Community structure
Microbial sharing
Commensal E. coli
Rhesus macaque
url https://peerj.com/articles/4271.pdf
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