Social information and socially transmitted pathogens are governed by social structure, and also shape social interactions. However, information and infection are rarely investigated as interactive factors driving social evolution. We propose exactly such an integrative framework, drawing attention to mechanisms of social phenotypic plasticity for information spread and pathogen control.
Lice are socially-transmitted ectoparasites. Transmission depends upon their host’s degree of contact with conspecifics. While grooming facilitates ectoparasite transmission via body contact, it also constrains their spread through parasite removal. We investigated relations between parasite burden and sociality in female Japanese macaques following two opposing predictions: i) central females in contact/grooming networks harbour more lice, related to their numerous contacts; ii) central females harbour fewer lice, related to receiving more grooming. We estimated lice load non-invasively using the conspicuous louse egg-picking behaviour performed by macaques during grooming. We tested for covariation in several centrality measures and lice load, controlling for season, female reproductive state and dominance rank. Results show that the interaction between degree centrality (number of partners) and seasonality predicted lice load: females interacting with more partners had fewer lice than those interacting with fewer partners in winter and summer, whereas there was no relationship between lice load and centrality in spring and fall. This is counter to the prediction that increased contact leads to greater louse burden but fits the prediction that social grooming limits louse burden. Interactions between environmental seasonality and both parasite and host biology appeared to mediate the role of social processes in louse burden.
Social structure can theoretically regulate disease risk by mediating exposure to pathogens via social proximity and contact. Investigating the role of central individuals within a network may help predict infectious agent transmission as well as implement disease control strategies, but little is known about such dynamics in real primate networks. We combined social network analysis and a modeling approach to better understand transmission of a theoretical infectious agent in wild Japanese macaques, highly social animals which form extended but highly differentiated social networks. We collected focal data from adult females living on the islands of Koshima and Yakushima, Japan. Individual identities as well as grooming networks were included in a Markov graph-based simulation. In this model, the probability that an individual will transmit an infectious agent depends on the strength of its relationships with other group members. Similarly, its probability of being infected depends on its relationships with already infected group members. We correlated: (i) the percentage of subjects infected during a latency-constrained epidemic; (ii) the mean latency to complete transmission; (iii) the probability that an individual is infected first among all group members; and (iv) each individual's mean rank in the chain of transmission with different individual network centralities (eigenvector, strength, betweenness). Our results support the hypothesis that more central individuals transmit infections in a shorter amount of time and to more subjects but also become infected more quickly than less central individuals. However, we also observed that the spread of infectious agents on the Yakushima network did not always differ from expectations of spread on random networks. Generalizations about the importance of observed social networks in pathogen flow should thus be made with caution, since individual characteristics in some real world networks appear less relevant than they are in others in predicting disease spread. Am. J. Primatol. 78:767-779, 2016. © 2016 Wiley Periodicals, Inc.
The capacity to use information provided by others to guide behavior is a widespread phenomenon in animal societies. A standard paradigm to test if and/or how animals use and transfer social information is through social diffusion experiments, by which researchers observe how information spreads within a group, sometimes by seeding new behavior in the population. In this article, we review the context, methodology and products of such social diffusion experiments. Our major focus is the transmission of information from an individual (or group thereof) to another, and the factors that can enhance or, more interestingly, inhibit it. We therefore also discuss reasons why social transmission sometimes does not occur despite being expected to. We span a full range of mechanisms and processes, from the nature of social information itself and the cognitive abilities of various species, to the idea of social competency and the constraints imposed by the social networks in which animals are embedded. We ultimately aim at a broad reflection on practical and theoretical issues arising when studying how social information spreads within animal groups.
Since group-living animals are embedded in a network of social interactions, socioecological factors may not only affect individual behavioral strategies but also the patterning of group-level social interactions, i.e., the network structure. These co-variations between socioecological factors, individual behavior, and group-level structure are important to study since ecological factors may strongly influence animal health outcomes and reproductive success. Besides factors such as social information and/or infectious agents, with far-reaching individual fitness consequences, seem independent of individuals' own social interactions but directly affected by the topology of the social network. This paper reviews how socio-ecological pressures, i.e., causal factors (food distribution, predation, and infectious agent risk), via intermediary mechanisms (stress, information sharing, and mating system), may affect individual social behavior and consequently, social network topology. We also discuss how evolutionary driving forces, genetic (i.e., genes) and cultural (i.e., learned behavior) selection, may result in a specific composition of individuals' social strategies that produce network topologies that might be optimized to specific socio-ecological conditions. We conclude that studies focusing on whether and how well networks resist changing conditions might provide a better understanding of the rules underlying individual behavior, which in turn influences network topology-a process we have called network evolution. Evolutionary processes may favor a group phenotypic composition, thus a network topology. This has been referred to as a "collective social niche construction".
Different hypotheses explain variation in the occurrence of self-directed behaviour such as scratching and self-grooming: a parasite hypothesis linked with ectoparasite load, an environmental hypothesis linked with seasonal conditions and a social hypothesis linked with social factors. These hypotheses are not mutually exclusive but are often considered separately. Here, we revisited these hypotheses together in female Japanese macaques (Macaca fuscata fuscata) of Kōjima islet, Japan. We input occurrences of scratching and self-grooming during focal observations in models combining parasitological (lice load), social (dominance rank, social grooming, aggression received and proximity), and environmental (rainfall, temperature and season) variables. Using an information-theory approach, we simultaneously compared the explanatory value of models against each other using variation in Akaike's information criterion and Akaike's weights. We found that evidence for models with lice load, with or without environmental–social parameters, was stronger than that for other models. In these models, scratching was positively associated with lice load and social grooming whereas self-grooming was negatively associated with lice load and positively associated with social grooming, dominance rank and number of female neighbours. This study indicates that the study animals scratch primarily because of an immune/stimulus itch, possibly triggered by ectoparasite bites/movements. It also confirms that self-grooming could act as a displacement activity in the case of social uncertainty. We advocate that biological hypotheses be more broadly considered even when investigating social processes, as one does not exclude the other.
Social structure can regulate information and pathogen transmission via social contact or proximity, which ultimately affects individual fitness. In theory, the same network properties that favor social information transmission also favor the spread of socially-transmitted pathogens, creating a tradeoff between them. The mechanisms underlying the development and stability of individual relationships considering this trade-off remain underexplored. Here, we outline the evolutionary mechanisms of social transmission and hypothesize that network topology can be optimized in a way that balances the costs and benefits of social relationships. In this context, emergent network properties might reflect a trade-off between information and pathogen transmission in animal societies. We then propose an implementation of Hinde's classical framework by incorporating the costs of socializing in a negative feedback loop in the emergence of social structure. We hope this manuscript encourages research into this underxplored social trade-off and the evolutionary processes underlying it.
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