Monkeys in the middle: parasite transmission through the social network of a wild primate

Abstract

In wildlife populations, group-living is thought to increase the probability of parasite transmission because contact rates increase at high host densities. Physical contact, such as social grooming, is an important component of group structure, but it can also increase the risk of exposure to infection for individuals because it provides a mechanism for transmission of potentially pathogenic organisms. Living in groups can also create variation in susceptibility to infection among individuals because circulating levels of immunosuppressive hormones like glucocorticoids often depend on an individual's position within the group's social structure. Yet, little is known about the relative roles of socially mediated exposure versus susceptibility in parasite transmission among free-living animal groups. To address this issue, we investigate the relationship between host dominance hierarchy and nematode parasite transmission among females in a wild group of Japanese macaques (Macaca fuscata yakui). We use social network analysis to describe each individual female's position within the grooming network in relation to dominance rank and relative levels of infection. Our results suggest that the number of directly-transmitted parasite species infecting each female, and the relative amount of transmission stages that one of these species sheds in faeces, both increase with dominance rank. Female centrality within the network, which shows positive associations with dominance hierarchy, is also positively associated with infection by certain parasite species, suggesting that the measured rank-bias in transmission may reflect variation in exposure rather than susceptibility. This is supported by the lack of a clear relationship between rank and faecal cortisol, as an indicator of stress, in a subset of these females. Thus, socially mediated exposure appears to be important for direct transmission of nematode parasites, lending support to the idea that a classical fitness trade-off inherent to living in groups can exist.

Figure 1. Sociograms illustrating the global social network (all seasons included) based on all recorded grooming given and received from a group of Yakushima macaques between October 2007 and August 2009.

Nodes represent individuals, with the size of the node representing the outward and inward eigenvector centrality scores for A and B, respectively. Node colour represents the three rank classes used in this study. Edges (lines) between individuals are weighted by strength, such that thicker lines indicate stronger grooming relationships. Arrow heads are also weighted by strength to indicate the magnitude and direction of grooming behaviour. Note that the degree of bias toward high ranking individuals is considerably stronger in the grooming received network, as indicated by larger discrepancies between the sizes of the nodes for each rank.

Figure 2. The relationship between dominance rank and eigenvector centrality in both the outward (Given) and inward (Received) grooming networks in female Yakushima macaques between October 2007 and August 2009.

Columns indicate the mean±SEM.

Figure 3. The relationship between dominance rank and parasite species richness in female Yakushima macaques between October 2007 and August 2009.

Columns indicate the mean±SEM.

Figure 4. The relationship between dominance rank and prevalence of infection by Oesophagostomum aculeatum across seasons in female Yakushima macaques between October 2007 and August 2009

. Columns indicate the mean±SEM.

Figure 5. The relationship between dominance rank and the number of Oesophagostomum aculeatum eggs shed in the faeces of female Yakushima macaques between October 2007 and August 2009.

Columns indicate the mean±SEM.

Figure 6. The relationship between dominance rank and faecal cortisol in female Yakushima macaques between October 2007 and August 2009.

Columns indicate the mean±SEM.