Affiliation and disease risk

social networks mediate gut microbial transmission among rhesus macaques

Krishna N. Balasubramaniam, Brianne Beisner, Josephine A. Hubbard, Jessica J. Vandeleest, Edward R Atwill, Brenda Mccowan

Research output: Contribution to journalArticle

Abstract

In social animals, affiliative behaviours bring many benefits, but also costs such as disease risk. The ways in which affiliation may affect the risk of infectious agent transmission remain unclear. Moreover, studies linking variation in affiliative interactions to infectious agent incidence/diversity have speculated that disease transmission may have occurred, rather than revealing that transmission did occur. We address these gaps using the phylogenetics of commensal gut Escherichia coli to determine whether affiliative grooming and huddling social networks mediated microbial transmission among rhesus macaques. We collected behavioural and microbial data from adult macaques across a 12-week period that was split into two 6-week phases to better detect dyadic transmission. We reconstructed undirected social networks from affiliative interactions and reconstructed microbial transmission networks from the pairwise phylogenetic similarity of E. coli pulsotypes from macaques within and across adjacent sampling events. Macaque E. coli pulsotypes were more phylogenetically similar to each other than to environmental isolates, which established a premise for socially mediated transmission. Dyadic grooming and huddling frequencies strongly influenced the likelihood of E. coli transmission during the second data collection phase, but not the first. Macaques that were more central/well connected in both their grooming and huddling networks were also more central in the E. coli transmission networks. Our results confirmed that affiliative grooming and huddling behaviours mediate the transmission of gut microbes among rhesus macaques, particularly among females and high-ranking individuals. The detectability of socially mediated E. coli transmission maybe partially masked by environmental acquisition in males, or by high frequencies of interactions in captivity. Predicting the potential transmission pathways of gastrointestinal parasites and pathogens, our findings add to current knowledge of the coevolutionary relationships between affiliative behaviour and health and may be used to identify ‘superspreader’ individuals as potential targets for disease control strategies.

Original languageEnglish (US)
Pages (from-to)131-143
Number of pages13
JournalAnimal Behaviour
Volume151
DOIs
StatePublished - May 1 2019

Fingerprint

grooming
social networks
social network
Macaca mulatta
intestinal microorganisms
affiliative behavior
grooming (animal behavior)
Escherichia coli
Macaca
phylogenetics
disease transmission
commensal
disease control
pathogens
captivity
digestive system
ranking
parasite
pathogen
phylogeny

Keywords

  • affiliative behaviour
  • commensal E. coli
  • infectious disease
  • rhesus macaque
  • social network
  • superspreader
  • transmission

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Animal Science and Zoology

Cite this

Affiliation and disease risk : social networks mediate gut microbial transmission among rhesus macaques. / Balasubramaniam, Krishna N.; Beisner, Brianne; Hubbard, Josephine A.; Vandeleest, Jessica J.; Atwill, Edward R; Mccowan, Brenda.

In: Animal Behaviour, Vol. 151, 01.05.2019, p. 131-143.

Research output: Contribution to journalArticle

Balasubramaniam, Krishna N. ; Beisner, Brianne ; Hubbard, Josephine A. ; Vandeleest, Jessica J. ; Atwill, Edward R ; Mccowan, Brenda. / Affiliation and disease risk : social networks mediate gut microbial transmission among rhesus macaques. In: Animal Behaviour. 2019 ; Vol. 151. pp. 131-143.
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