Social bufferingandcontact transmission: network connections have beneficial and detrimental effects onShigellainfection risk among captive rhesus macaques

Abstract

In social animals, group living may impact the risk of infectious disease acquisition in two ways. On the one hand, social connectedness puts individuals at greater risk or susceptibility for acquiring enteric pathogens via contact-mediated transmission. Yet conversely, in strongly bonded societies like humans and some nonhuman primates, having close connections and strong social ties of support can also socially buffer individuals against susceptibility or transmissibility of infectious agents. Using social network analyses, we assessed the potentially competing roles of contact-mediated transmission and social buffering on the risk of infection from an enteric bacterial pathogen (Shigella flexneri) among captive groups of rhesus macaques (Macaca mulatta). Our results indicate that, within two macaque groups, individuals possessing more direct and especially indirect connections in their grooming and huddling social networks were less susceptible to infection. These results are in sharp contrast to several previous studies that indicate that increased (direct) contact-mediated transmission facilitates infectious disease transmission, including our own findings in a third macaque group in which individuals central in their huddling network and/or which initiated more fights were more likely to be infected. In summary, our findings reveal that an individual’s social connections may increase or decrease its chances of acquiring infectious agents. They extend the applicability of the social buffering hypothesis, beyond just stress and immune-function-related health benefits, to the additional health outcome of infectious disease resistance. Finally, we speculate that the circumstances under which social buffering versus contact-mediated transmission may occur could depend on multiple factors, such as living condition, pathogen-specific transmission routes, and/or an overall social context such as a group’s social stability.

Exposure and susceptibility drive reinfection with gastrointestinal parasites in a social primate

“…In contrast, opposite‐sex bond strength was not closely related to number of grooming partners (Pearson correlation: R = 0.10, p = 0.93). Similarly, high network integration has been shown to be either protective or a risk factor to GI parasite infections in captive macaques (Balasubramaniam, Beisner, Vandeleest, Atwill, & McCowan, ), highlighting the dual function of sociality. Another possibility is that the female propensity to form strong bonds with close kin (Silk, Alberts, & Altmann, ) leads to frequent contacts between genetically similar individuals potentially more similar in susceptibility or exposure than unrelated individuals.…”

“…Parasite transmission often has a social component (Balasubramaniam et al, ; Drewe, ; MacIntosh et al, ), but is not always linked to direct contact (Friant et al, ; Grear, Luong, & Hudson, ), suggesting parasite‐specific patterns, for example different transmission pathways in parasites with mobile (free‐living larvae) versus immobile (embryonated eggs) infective stages (MacIntosh et al, ). In vervet monkeys and our study, grooming many different partners increased infection risk with GI nematodes (Wren et al, ), indicating a social component of transmission.…”

Three Hypergraph Eigenvector Centralities

“…The vector c gives the centrality scores, which are unique up to scaling. Eigenvector centrality of this form has appeared in a range of applications, including the analysis of infectious disease spreading in primates [Balasubramaniam et al, 2016], patterns in fMRI data of human brains [Lohmann et al, 2010], and career trajectories of Hollywood actors [Taylor et al, 2017].…”

“…This means that the graph induced by M is undirected and "strongly connected" really just means "connected." Furthermore, the graph induced by M has the same connectivity as the clique expansion graph of a hypergraph [Agarwal et al, 2006], where each hyperedge induces a clique on the nodes in the graph. There are natural notions of directed hypergraphs with non-symmetric adjacency tensors [Gallo et al, 1993], and some of the theorems we use later still apply in these cases.…”

Primate Infectious Disease Ecology: Insights and Future Directions at the Human-Macaque Interface

“…In wild Japanese macaques, for instance, high-ranking individuals with more direct and indirect connections, or eigenvector centrality (Newman 2006) in their social grooming networks, were also shown to have greater species richness and infection intensities of nematode parasites (MacIntosh et al 2012). Yet having strong and diverse social connections, rather than increasing parasite acquisition owing to contact-mediated transmission, may actually decrease the likelihood of such acquisition by mitigating stressors or enhancing immune function (e.g., Balasubramaniam et al 2016;Cohen et al 2015;Fig. 13.3 Hypothetical social (a), bipartite (b), and multimodal (c) networks of the same individuals.…”