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.

Brown spider monkeys ( Ateles hybridus ): a model for differentiating the role of social networks and physical contact on parasite transmission dynamics

“…Social interactions that involve close proximity or physical contact between group members (e.g. grooming, huddling, mating, biting) can be used by parasites and pathogens as direct transmission pathways to spread through host populations [9][10][11][12] (reviewed in [1,2,13]). Therefore, generally, it has been predicted that higher levels of social interaction are associated with higher levels of transmission for directly transmitted parasites and pathogens, (e.g.…”

“…However, empirical evidence shows that gastrointestinal parasites, which usually have indirect transmission pathways, can also be transmitted through social interactions (e.g. during grooming, when infectious stages are ingested by the grooming actor from the fur of the grooming recipient [9,11]). …”

Evaluating empirical contact networks as potential transmission pathways for infectious diseases

“…Interface 13: 20160166 degree is a significant predictor of infection status. These methods were selected because they represent commonly used approaches for assessing the importance of network connectivity on infection patterns [2,10,34,35]. Monte Carlo p-values based on random re-assortments of individuals across nodes were used in both tests.…”

Intestinal parasite communities of six sympatric lemur species at Kirindy Forest, Madagascar

“…in P. verreauxi was around 90 %, and this nematode relies on larval development in the environment to become infectious. Active host-seeking behavior and nictation, i.e., raising of the body in response to olfactory cues, may aid the infectious larvae of this parasite to cling to the hosts' fur during limited ground contact events, and facilitate their spread through the population via direct animal-to-animal contact and grooming (Lee, 2002;MacIntosh et al, 2012;Springer, 2015).…”