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      Markedly Elevated Antibody Responses in Wild versus Captive Spotted Hyenas Show that Environmental and Ecological Factors Are Important Modulators of Immunity

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          Abstract

          Evolutionary processes have shaped the vertebrate immune system over time, but proximal mechanisms control the onset, duration, and intensity of immune responses. Based on testing of the hygiene hypothesis, it is now well known that microbial exposure is important for proper development and regulation of the immune system. However, few studies have examined the differences between wild animals in their natural environments, in which they are typically exposed to a wide array of potential pathogens, and their conspecifics living in captivity. Wild spotted hyenas ( Crocuta crocuta) are regularly exposed to myriad pathogens, but there is little evidence of disease-induced mortality in wild hyena populations, suggesting that immune defenses are robust in this species. Here we assessed differences in immune defenses between wild spotted hyenas that inhabit their natural savanna environment and captive hyenas that inhabit a captive environment where pathogen control programs are implemented. Importantly, the captive population of spotted hyenas was derived directly from the wild population and has been in captivity for less than four generations. Our results show that wild hyenas have significantly higher serum antibody concentrations, including total IgG and IgM, natural antibodies, and autoantibodies than do captive hyenas; there was no difference in the bacterial killing capacity of sera collected from captive and wild hyenas. The striking differences in serum antibody concentrations observed here suggest that complementing traditional immunology studies, with comparative studies of wild animals in their natural environment may help to uncover links between environment and immune function, and facilitate progress towards answering immunological questions associated with the hygiene hypothesis.

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          Allergy, parasites, and the hygiene hypothesis.

          The increase of allergic diseases in the industrialized world has often been explained by a decline in infections during childhood. The immunological explanation has been put into the context of the functional T cell subsets known as T helper 1 (TH1) and T helper 2 (TH2) that display polarized cytokine profiles. It has been argued that bacterial and viral infections during early life direct the maturing immune system toward TH1, which counterbalance proallergic responses of TH2 cells. Thus, a reduction in the overall microbial burden will result in weak TH1 imprinting and unrestrained TH2 responses that allow an increase in allergy. This notion is contradicted by observations that the prevalence of TH1-autoimmune diseases is also increasing and that TH2-skewed parasitic worm (helminth) infections are not associated with allergy. More recently, elevations of anti-inflammatory cytokines, such as interleukin-10, that occur during long-term helminth infections have been shown to be inversely correlated with allergy. The induction of a robust anti-inflammatory regulatory network by persistent immune challenge offers a unifying explanation for the observed inverse association of many infections with allergic disorders.
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            Sex differences in autoimmune disease.

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              Heritable true fitness and bright birds: a role for parasites?

              Combination of seven surveys of blood parasites in North American passerines reveals weak, highly significant association over species between incidence of chronic blood infections (five genera of protozoa and one nematode) and striking display (three characters: male "brightness," female "brightness," and male song). This result conforms to a model of sexual selection in which (i) coadaptational cycles of host and parasites generate consistently positive offspring-on-parent regression of fitness, and (ii) animals choose mates for genetic disease resistance by scrutiny of characters whose full expression is dependent on health and vigor.
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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, CA USA )
                1932-6203
                7 October 2015
                2015
                : 10
                : 10
                : e0137679
                Affiliations
                [1 ]Menzies Research Institute Tasmania, University of Tasmania, Hobart, TAS, Australia
                [2 ]Department of Zoology, Michigan State University, East Lansing, MI, United States of America
                [3 ]Interdisciplinary program in Ecology, Evolutionary Biology and Behavior, Michigan State University, East Lansing, MI, United States of America
                [4 ]Department of Pharmacy and Medical Sciences, University of South Australia, Adelaide, South Australia, Australia
                [5 ]Department of Microbiology and Molecular Genetics, National Food Safety and Toxicology Center, Michigan State University, East Lansing, MI, United States of America
                [6 ]Custom Monoclonals International Corp, West Sacramento, CA, United States of America
                [7 ]Department of Psychology, University of California, Berkeley, CA, United States of America
                King's College London, UNITED KINGDOM
                Author notes

                Competing Interests: The authors have the following competing interests. Chris K. Grant is president of Custom Monoclonals International, which contributed antibodies for this research. There are no patents, products in development or marketed products to declare. This does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials, as detailed online in the guide for authors.

                Conceived and designed the experiments: ASF LSM CKG KEH. Performed the experiments: ASF MLW. Analyzed the data: ASF LSM KEH. Contributed reagents/materials/analysis tools: ASF LSM CKG KEH MLW. Wrote the paper: ASF LSM CKG KEH. Submitted the manuscript: ASF.

                Article
                PONE-D-15-15860
                10.1371/journal.pone.0137679
                4621877
                26444876
                2a5a70e2-31bc-4cbf-a878-dae7dccc57fb
                Copyright @ 2015

                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
                : 15 April 2015
                : 19 August 2015
                Page count
                Figures: 5, Tables: 1, Pages: 18
                Funding
                This work was supported by Award No.W911NF-08-1-0310 from the Army Research Office, National Institutes of Health grant 1R01GM105042, and National Science Foundation grants IOS1121474 and DEB1353110 to KEH, National Science Foundation Grant IOS0809914 to Stephen Glickman, National Institutes of Health grants K26RR023080 and U10 AI090872 to LSM, Grants-in-Aid-of research from Sigma Xi, Grants-in-Aid of Research from the American Society of Mammalogists, Veterinary Student Scholars grant D12Z0-604 from the Morris Animal Foundation, and an NSF Graduate Research Fellowship to ASF. Custom Monoclonals International Corp contributed antibodies used in this study. Author CKG, president of Custom Monoclonals International Corp, provided advice on experimental design, assay optimization, and assisted in writing the Materials and Methods section of the manuscript. The specific role of this author is articulated in the ‘author contributions’ section.
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