Gregariousness is associated with parasite species richness in a community of wild chimpanzees

Abstract

Increased risk of pathogen transmission through proximity and contact is a well-documented cost of sociality. Affiliative social contact, however, is an integral part of primate group life and can benefit health. Despite its importance to the evolution and maintenance of sociality, the tradeoff between costs and benefits of social contact for group-living primate species remains poorly understood. To improve our understanding of this interplay, we used social network analysis to investigate whether contact via association in the same space and/or physical contact measured through grooming were associated with helminth parasite species richness in a community of wild chimpanzees (Pan troglodytes schweinfurthii). We identified parasite taxa in 381 fecal samples from 36 individuals from the Kasekela community of chimpanzees in Gombe National Park, Tanzania, from November 1, 2006, to October 31, 2012. Over the study period, eight environmentally transmitted helminth taxa were identified. We quantified three network metrics for association and grooming contact, including degree strength, betweenness, and closeness. Our findings suggest that more gregarious individuals-those who spent more time with more individuals in the same space-had higher parasite richness, while the connections in the grooming network were not related to parasite richness. The expected parasite richness in individuals increased by 1.13 taxa (CI: 1.04, 1.22; p = 0.02) per one standard deviation increase in degree strength of association contact. The results of this study add to the understanding of the role that different types of social contact play in the parasite richness of group-living social primates. Significance statementParasite infections reveal costs of group living among wild animal populations. We studied the relationship between sociality and parasite transmission by assessing whether variation in social behavior among wild chimpanzees is associated with the number of unique helminth parasites detected in individual fecal samples. Our findings revealed that associating in the same shared space, but not grooming contact, is related to higher parasite richness. These findings improve our understanding of the complex interplay of parasitism and sociality with important implications for parasite transmission patterns in host species with flexible grouping patterns.

Respiratory Disease Risk of Zoo-Housed Bonobos Is Associated with Sex and Betweenness Centrality in the Proximity Network

“…In addition, degree and betweenness centrality predicted helminth infection in a proximity network of red-capped mangabeys ( Cercocebus torquatus ) [ 52 ]. Finally, strength in an association network based on same-subgroup membership predicted parasite richness in a group of chimpanzees ( Pan troglodytes ) [ 53 ]. Taken together, these studies appear to indicate a strong influence of individual differences in social-network position on parasite infection risk in primates.…”

Association of human disturbance and gastrointestinal parasite infection of yellow baboons in western Tanzania

“…We found group size to be associated with prevalence of some parasite taxa, mostly protozoans, which results from increased animal density and exposure risk amongst larger groups [ 78 ]. While sociality, the tendency to form social living groups, has many benefits for wild NHPs [ 79 ], increased risk of parasite infection is one well-documented cost [ 80 , 81 ], with spatial cohesion and contact between individual hosts facilitating parasite transmission [ 82 , 83 ]. Larger group size may also be associated with higher parasite prevalence due to increased resource competition between group members and social stress amongst host individuals [ 33 , 84 ] leading to poor nutrition and thus increased parasite susceptibility.…”

Sociality and disease: behavioral perspectives in ecological and evolutionary immunology

“…(b) Disease and social structure/network Several articles in this collection leverage social structure and network analyses to provide insights into the role of behavioral interactions on disease transmissibility. Deere et al (2021), for example, found that wild chimpanzees that spent more time with more individuals in the same area had higher helminth parasite richness, concluding that same shared space, rather than grooming contact, is responsible for higher parasitic risk. However, Lynsdale et al (2022) failed to find an association between gastrointestinal nematode load and sociality (measured by individual solitary behavior, work group size, and work group sex ratio) in semi-captive Asian elephants employed in timber logging.…”