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      Monkeys in the Middle: Parasite Transmission through the Social Network of a Wild Primate

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          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.

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          The effects of hormones on sex differences in infection: from genes to behavior.

          S L Klein (2000)
          Males of many species are more susceptible than females to infections caused by parasites, fungi, bacteria, and viruses. One proximate cause of sex differences in infection is differences in endocrine-immune interactions. Specifically, males may be more susceptible to infection than females because sex steroids, specifically androgens in males and estrogens in females, modulate several aspects of host immunity. It is, however, becoming increasingly more apparent that in addition to affecting host immunity, sex steroid hormones alter genes and behaviors that influence susceptibility and resistance to infection. Thus, males may be more susceptible to infection than females not only because androgens reduce immunocompetence, but because sex steroid hormones affect disease resistance genes and behaviors that make males more susceptible to infection. Consideration of the cumulative effects of sex steroid hormones on susceptibility to infection may serve to clarify current discrepancies in the literature and offer alternative hypotheses to the view that sex steroid hormones only alter susceptibility to infection via changes in host immune function.
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            Infection in social networks: using network analysis to identify high-risk individuals.

            Simulation studies using susceptible-infectious-recovered models were conducted to estimate individuals' risk of infection and time to infection in small-world and randomly mixing networks. Infection transmitted more rapidly but ultimately resulted in fewer infected individuals in the small-world, compared with the random, network. The ability of measures of network centrality to identify high-risk individuals was also assessed. "Centrality" describes an individual's position in a population; numerous parameters are available to assess this attribute. Here, the authors use the centrality measures degree (number of contacts), random-walk betweenness (a measure of the proportion of times an individual lies on the path between other individuals), shortest-path betweenness (the proportion of times an individual lies on the shortest path between other individuals), and farness (the sum of the number of steps between an individual and all other individuals). Each was associated with time to infection and risk of infection in the simulated outbreaks. In the networks examined, degree (which is the most readily measured) was at least as good as other network parameters in predicting risk of infection. Identification of more central individuals in populations may be used to inform surveillance and infection control strategies.
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              Contact Networks in a Wildlife-Livestock Host Community: Identifying High-Risk Individuals in the Transmission of Bovine TB among Badgers and Cattle

              Background The management of many pathogens, which are of concern to humans and their livestock, is complicated by the pathogens' ability to cross-infect multiple host species, including wildlife. This has major implications for the management of such diseases, since the dynamics of infection are dependent on the rates of both intra- and inter-specific transmission. However, the difficulty of studying transmission networks in free-living populations means that the relative opportunities for intra- versus inter-specific disease transmission have not previously been demonstrated empirically within any wildlife-livestock disease system. Methodology/Principal Findings Using recently-developed proximity data loggers, we quantify both intra-and inter-specific contacts in a wildlife-livestock disease system, using bovine tuberculosis (bTB) in badgers and cattle in the UK as our example. We assess the connectedness of individuals within the networks in order to identify whether there are certain ‘high-risk’ individuals or groups of individuals for disease transmission within and between species. Our results show that contact patterns in both badger and cattle populations vary widely, both between individuals and over time. We recorded only infrequent interactions between badger social groups, although all badgers fitted with data loggers were involved in these inter-group contacts. Contacts between badgers and cattle occurred more frequently than contacts between different badger groups. Moreover, these inter-specific contacts involved those individual cows, which were highly connected within the cattle herd. Conclusions/Significance This work represents the first continuous time record of wildlife-host contacts for any free-living wildlife-livestock disease system. The results highlight the existence of specific individuals with relatively high contact rates in both livestock and wildlife populations, which have the potential to act as hubs in the spread of disease through complex contact networks. Targeting testing or preventive measures at high-contact groups and individuals within livestock populations would enhance the effectiveness and efficiency of disease management strategies.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                5 December 2012
                : 7
                : 12
                : e51144
                Affiliations
                [1 ]Center for International Collaboration and Advanced Studies in Primatology, Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan
                [2 ]Département Ecologie, Physiologie et Ethologie, Institut Pluridisciplinaire Hubert Curien Centre National de la Recherche Scientifique UMR7178, Université de Strasbourg, Strasbourg, Alsace, France
                [3 ]Laboratoire de Dynamique de l’Évolution Humaine, Centre National de la Recherche Scientifique UPR 2147, Paris, Île-de-France, France
                [4 ]Department of Zoology, Faculty of Science, Okayama University of Science, Okayama City, Okayama, Japan
                [5 ]Center for Infectious Disease Dynamics, The Pennsylvania State University, University Park, Pennsylvania, United States of America
                University of Osnabrueck, Germany
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AJJM ADH AJ. Performed the experiments: AJJM CG KM. Analyzed the data: AJJM AJ. Wrote the paper: AJJM ADH. Contributed substantially to supervision and discussion: MAH KS.

                Article
                PONE-D-12-17083
                10.1371/journal.pone.0051144
                3515516
                23227246
                6dd4e22c-843f-4574-a3fb-edf32a2402d0
                Copyright @ 2012

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 8 June 2012
                : 31 October 2012
                Page count
                Pages: 12
                Funding
                A. J. J. MacIntosh was financially supported by the Japan Ministry of Education, Culture, Sports, Science and Technology (MEXT, http://www.mext.go.jp/english/: Monbukagakusho scholarship), A. Jacobs and C. Garcia by a grant from the French Ministry of Higher Education and Research, and C. Garcia and A. D. Hernandez by a Japan Society for the Promotion of Science (JSPS, http://www.jsps.go.jp/english/) postdoctoral fellowship, inclusive of Grants-in-Aid from JSPS to M. A. Huffman. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Ecology
                Ecological Metrics
                Species Diversity
                Species Richness
                Behavioral Ecology
                Evolutionary Biology
                Evolutionary Processes
                Coevolution
                Animal Behavior
                Behavioral Ecology
                Model Organisms
                Animal Models
                Macaque
                Theoretical Biology
                Zoology
                Helminthology
                Mammalogy
                Nematology
                Parasitology
                Social and Behavioral Sciences
                Anthropology
                Biological Anthropology
                Sociology
                Social Networks
                Veterinary Science
                Veterinary Epidemiology

                Uncategorized
                Uncategorized

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