Browsing by Subject "Hormones"

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 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 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.

Much of our knowledge of the mammalian immune system comes from laboratory studies of model organisms in highly controlled settings; however, in nature, organisms experience myriad biotic and abiotic pressures that can influence the immune response. Understanding how the immune system operates in natural systems therefore requires studies of animals living in socially and ecologically relevant environments. Here, I investigated the drivers of individual variation in immunocompetence in a wild population of meerkats (Suricata suricatta) living in the Kalahari Desert. The meerkat is characterised by aggressively mediated female social dominance, and although hormonal masculinization is present to varying degrees in all adult, female meerkats, the dominant female in each clan has greater concentrations of total androgens than does any other clan member. I therefore tested if the immunocompetence handicap hypothesis (ICHH), which posits that androgens in males mediate a trade off between reproductive success and immunocompetence, could apply to females and perhaps extend to their offspring. From 2012-2015, I followed and sampled approximately 300 meerkats living in 24 social clans. I related measures of immunocompetence (i.e., gastrointestinal parasite burdens and innate immune function) to environmental, demographic, social, and endocrine variables. I tested for transgenerational effects of maternally derived androgens on offspring immunocompetence by administering an antiandrogen to pregnant dominant dams. For adult meerkats, I found that there is a cost to dominance, in terms of reduced immunocompetence and that those with greater androgen concentrations (either inferred from fecal androgen metabolites or measured directly from blood as androstenedione, A4) had greater parasite burdens and weaker immune responses. Because, in female meerkats, A4 appears to exert the dual effects of promoting reproductive success and compromising immunity, I propose that the ICHH can apply to females. Moreover, the immunosuppressive consequences of female hormonal masculinization extend beyond the dams to their offspring, via prenatal exposure to raised androgens, and therefore may represent a transgenerational consequence of sexual selection operating in females. By studying immune function in natural systems, we can gain a broader perspective on immune function from an ecological and evolutionary context.

Sexual conflict occurs when female and male fitness interests diverge. In a social system characterized by aggressive sexual coercion and the risk of infanticide, female chimpanzees (Pan troglodytes) respond to this conflict by exhibiting an exaggerated sexual swelling that advertises sexual receptivity while concealing the exact timing of ovulation. Sexual swellings impose significant costs, yet can persist into pregnancy. Records from long-term studies of eastern chimpanzees (P. t. schweinfurthii) in Gombe National Park, TZ, and Kibale National Park, UG, provide data on postconception swellings, while data on group composition and behaviors such as mating, grooming, and aggression are drawn from the Gombe database only. Throughout, I use linear mixed models to simultaneously test multiple effects while controlling for repeated measures of individuals. In Chapter 1, I tested whether variation in females’ vulnerability to infanticide and aggression predicted the amount of swelling during pregnancy. In Chapter 2, I examined female-male relationships across reproductive states to ask whether females can better gain benefits and avoid costs by affiliating promiscuously with all males, or by investing in relationships with preferred males. Finally, I analyzed metabolites of reproductive hormones using urine samples from pregnant females in both populations to build a hormonal profile of postconception swellings. Swellings during pregnancy increase female-male association, and are caused by the same basic hormonal mechanism as preconception swellings, though they occur in a very different hormonal milieu. Females at greater risk of infanticide and intrasexual aggression swell more during pregnancy. Females mate promiscuously before conception, but during pregnancy and lactation, preferentially groom with males that are likely to protect them from aggression and infanticide. Based on these and other findings, I conclude that postconception swellings in chimpanzees are an adaptive response to sexual conflict.

Organismal form emerges from the relative growth of the body and its parts. In this dissertation, I address how developmental processes produce the size relationships between body parts that shape the characteristic morphologies of animals and plants. Specifically, I study the nutrition-dependent growth of wings in butterflies and moths to determine the developmental physiological mechanisms underlying morphological scaling relationships. Additionally, I dive into how form within a tissue is established by studying the mechanism that patterns growth of butterfly wings. Using an extensive data set from rats fed on a low protein diet, I analyze how different bones respond to nutritional variation and its effect on morphological integration. Finally, I end with a theoretical chapter discussing the ways in which development can be plastic and how that shapes both genetic and phenotypic evolution. I find that developmental plasticity emerges from changes in the concentration of systemic hormones in response to environmental stimuli. Hormones, in turn, interact with every developing part. This interaction is characterized by character-specific gene regulatory networks that affect their sensitivity to hormones. Thus, developmental plasticity emerges from the interplay between the organism sensing the environment that tunes the strength of a systemic signal that moderates development, and character-specific use of molecular networks that defines the range of character states in response to signal variation.

Female social dominance over males is unusual in mammals, yet characterizes most Malagasy lemurs, which represent almost 30% of all primates. Despite its prevalence in this suborder, both the evolutionary trajectory and proximate mechanism of female dominance remain unclear. Potentially associated with female dominance is a suite of behavioral, physiological and morphological traits in females that implicates ‘masculinization’ via androgen exposure; however, relative to conspecific males, female lemurs curiously show little evidence of raised androgen concentrations. In order to illuminate the proximate mechanisms underlying female dominance in lemurs, I observed mixed‐sex pairs of related Eulemur species, and identified two key study groups ‐‐ one comprised of species expressing female dominance and, the other comprised of species (from a recently evolved clade) showing equal status between the sexes (hereafter ‘egalitarian’). Comparing females from these two groups, to test the hypothesis that female dominance is an expression of an overall masculinization of the female, I 1) characterize the expression of female dominance, aggression, affiliation, and olfactory communication in Eulemur; 2) provide novel information about the hormonal and neuroendocrine correlates associated with the expression of female dominance; 3) investigate the activational role of the sex-steroid hormones in adult female Eulemur using seasonal correlates of hormonal and behavioral change; and 4) examine the specific role of estrogen in the regulation and expression of sex-reversed female behavior in these species. In doing so I highlight significant behavioral and physiological differences between female-dominant and egalitarian Eulemur and show that female dominance is associated with a more masculine behavioral and hormonal profile. I also suggest that these behavioral and hormonal differences may be the result of fundamental differences in the biosynthetic pathway associated with estrogen production. Moreover, I assert that these putative physiological differences could provide a parsimonious proximate mechanism explaining the evolution of female dominance and its subsequent relaxation in egalitarian Eulemur species.