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View / Download 2.7 Mb Disease Risk in Wild Primate Populations: Host and Environmental Predictors, Immune Responses and Costs of Infection by Mercy Yvonne Akinyi Department of Biology Duke University Date: _______________________ Approved: ___________________________ Susan Alberts, Supervisor ___________________________ Elizabeth Archie ___________________________ Charles Nunn ___________________________ Katharina Koelle ___________________________ Jenny Tung Dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Biology in the Graduate School of Duke University 2017 i v ABSTRACT Disease Risk in Wild Primate Populations: Host and Environmental Predictors, Immune Responses and Costs of Infection by Mercy Yvonne Akinyi Department of Biology Duke University Date: _______________________ Approved: ___________________________ Susan Alberts, Supervisor ___________________________ Elizabeth Archie ___________________________ Charles Nunn ___________________________ Katharina Koelle ___________________________ Jenny Tung An abstract of a dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Biology in the Graduate School of Duke University 2017 Copyright by Mercy Yvonne Akinyi 2017 Abstract Disease risk in wild animal populations is driven by multiple factors, including host, parasite, and environmental traits, that facilitate the transmission of parasites and infection of hosts. Parasites inflict costs on their hosts that affect host fitness with downstream consequences on population structures and disease emergence patterns. Most disease risk-related studies are conducted in captive animals, while few have focused on free-ranging populations because of the logistical challenges associated with long-term monitoring of the hosts and sample collection. Hence, data regarding disease dynamics in natural populations are scarce, which limits our understanding of the ecological and evolutionary context of disease dynamics. In this thesis, we investigate the forces driving disease risk in wild primates and the possible consequences of infection on these hosts. We used longitudinal and cross-sectional data sets from wild primate populations in Kenya, Eastern Africa, to examine the following aims: 1) the effect of host behavior on hormones associated with disease risk, 2) environmental and host factors that predispose individuals to helminth infections, and 3) the immune responses and fitness costs associated with helminth infections. First, we investigated how two maturational milestones in wild male baboons—natal dispersal and rank attainment— were associated with variation in fecal hormone metabolites (glucocorticoids and testosterone). These two hormones are generally considered to be immunosuppressive iv and are often associated with high parasite loads. Within this analysis, we also investigated whether changes in the frequencies of behaviors (mating and agonistic encounters) were associated with adult dominance rank attainment. Second, we investigated multiple sources of variance in helminth burdens in a well-studied population of wild female baboons, including factors that contribute to both exposure and susceptibility (group size, social status, rainfall, temperature, age, and reproductive status). Third, we investigated how hematological indices and body mass index were associated with helminth burden. In the first study, our results revealed that rank attainment is associated with an increase in fecal glucocorticoids (fGC) levels but not fecal testosterone (fT) levels: males that have achieved an adult rank have higher fGC than males that have not yet attained an adult rank. We also found that males win more agonistic encounters and acquire more reproductive opportunities after they have attained adult rank than before they have done so. The second study revealed that female baboons in Amboseli were infected with diverse helminth taxa, including both directly transmitted and indirectly transmitted helminths. In general, high parasite risk was linked to large group sizes, low rainfall conditions, old age, and pregnancy, although these predictors varied somewhat across helminth species. Fecal GC levels were not associated with any measures of helminth burden. The third study found that helminth burdens were positively associated with circulating lymphocyte counts and negatively associated with v neutrophil-lymphocyte ratios (NLR). We did not find any associations between helminth burdens and total WBC or eosinophil counts. Red blood cell indices were not predicted by our measures of helminth burden but instead varied with age class and sex. Helminth burdens were also negatively correlated with body mass index (BMI). Overall, the findings of this thesis are consistent with the hypothesis that host and environmental traits are important predictors of disease risk and infection in wild primate populations. In addition, our results suggest that wild primates mount immune responses to helminth burden and that helminth infections may have detrimental consequences on host body condition. Our work enhances the limited data on sources of disease variation and associated costs in wild populations. It also emphasizes the continued need for disease surveillance and health monitoring in wild populations. vi Dedication This dissertation is dedicated to my beloved family and friends without whom I would not have achieved this important milestone. “What lies behind us and what lies before us are small matters compared to what lies within us. And when we bring what is within us out into the world, miracles happen.” Ralph Waldo Emerson (1803-1882) vii Contents Abstract ......................................................................................................................................... iv List of Tables ............................................................................................................................... xiii List of Figures ............................................................................................................................. xiv Acknowledgements .................................................................................................................... xv 1. Introduction ................................................................................................................................ 1 1.1 Background ........................................................................................................................ 1 1.2 Behavior, hormones and disease risk ............................................................................. 2 1.3 Determinants of helminth infections .............................................................................. 4 1.4 Immune responses and costs of helminth infections ................................................... 7 1.5 Wild primates as a study model ..................................................................................... 8 1.6 Thesis objectives .............................................................................................................. 10 2. Hormonal correlates of natal dispersal and rank attainment in wild male baboons. ... 13 2.1 Introduction ..................................................................................................................... 13 2.1.1 Maturational milestones, glucocorticoids and testosterone ................................ 14 2.1.2. Goals, hypotheses and predictions ......................................................................... 19 2.2 Methods ............................................................................................................................ 20 2.2.1 Study population ........................................................................................................ 20 2.2.2 Study subjects, maturational milestones and behavioral data ............................ 20 2.2.3 Fecal sample collection, hormone extraction, validation and analyses ............. 21 2.2.4 Data analysis ............................................................................................................... 22 viii 2.2.4.1 Analysis of variation in fGC and fT metabolites associated with natal dispersal and rank attainment ...................................................................................... 22 2.2.4.2 Analysis of variation in mating and agonistic encounters before and after adult rank attainment..................................................................................................... 25 2.3 Results ............................................................................................................................... 27 2.3.1 Analysis of variation in fGC and fT metabolites associated with natal dispersal and rank attainment............................................................................................................ 27 2.3.2 Analysis of variation in mating and aggression before and after rank attainment ............................................................................................................................ 30 2.4 Discussion......................................................................................................................... 32 3. Environmental and host-specific predictors of helminth burden in female baboons. .. 38 3.1 Introduction ....................................................................................................................
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