Browsing by Author "Alberts, Susan C"

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.

In many species, early life experiences have striking effects on health, reproduction, and survival in adulthood. Thus, early life conditions shape a range of evolutionarily relevant traits, and in doing so alter the genotype-phenotype relationship and the phenotypic distribution on which selection acts. Because of the key role early life effects play in generating variation in fitness-related traits, understanding their evolution and mechanistic basis is crucial. To gain traction on these topics, my dissertation draws on ecological, demographic, and genomic data from a long-term study population of wild baboons in Amboseli, Kenya to address three major themes: (i) the adaptive significance of early life effects, (ii) the molecular mechanisms that connect early life experiences with later life traits, and (iii) the development of laboratory tools for understanding the role of one particular mechanism—DNA methylation—in translating environmental inputs into phenotypic variation. In chapter one, I empirically test two competing explanations for how early life effects evolve, providing novel insight into the evolution of developmental plasticity in long-lived species. In chapter two, I address the degree to which ecological effects on fitness-related traits are potentially mediated by changes in DNA methylation. Finally, in chapter three, I develop a high-throughput assay to improve our knowledge of the phenotypic relevance of changes in the epigenome. Together, this work provides some of the first empirical data on the genes and mechanisms involved in sensing and responding to environmental variation in wild mammals, and more generally addresses several critical gaps in our understanding of how early experiences affect evolutionarily relevant traits.

Forest elephants (Loxodonta cyclotis), the smallest and least studied of the three extant elephant species, predominately inhabit the Guinean and Congolian tropical forests from Guinea to the Democratic Republic of Congo. Known as ecosystem engineers, forest elephants create and maintain forest habitat, shape faunal communities, transport nutrients, and disperse seeds to distant areas. Despite their essential ecological role, very little is known about forest elephant social behavior. Living in social groups provides individuals with many benefits, including information about resources, protection from predators, and access to mates. For highly social species, like elephants, understanding social behavior is crucial to implementing sustainable conservation practices and mitigating the negative impacts of human development. To date, what is known about forest elephant social behavior originates from observations in baïs – mineral rich forest clearings. As a result, our understanding is limited by the short periods of time forest elephants spend in baïs, less than 2% of their time, and the small area relative to the rest of their home range and lifespan that we are able to observe. In this dissertation, I present research from the first project to attempt to understand elephant social interactions from throughout the range of habitats that forest elephants exploit on a daily basis, including dense, closed-canopy forest. I combine genetic and satellite technologies (GPS tracking and remote sensing) using novel computational methods to address: (1) factors that influence fluctuations in forest elephant group size; (2) forest elephant group age-sex composition and the factors influencing the probability of interactions between two elephants; and (3) improvements to forest elephant monitoring via line transect surveys for dung by creating an adaptive dung decay model. I conclude that: (1) group size is variable with forest elephants displaying a fission-fusion social system – a flexible social system in which individuals or sub-groups intermittently join other groups – across habitats in response to fruit availability and human disturbance; (2) interaction between individuals is influenced by social, but not environmental, factors and forest elephants spend more time in mixed sex groups than Asian or savanna elephants; and (3) estimating dung degradation via remotely sensed imagery is a feasible, cost-efficient alternative or supplement to in-situ dung degradation studies for non-invasive population surveys. This dissertation highlights the value of untangling the complex interplay between environmental, social, and anthropogenic drivers of species group composition and social behavior to inform conservation action., the results herein will be informative for monitoring forest elephant populations and promoting human-elephant coexistence through improved management of potential conflict areas.

Although evolution results from differential reproduction and survival at the level of the individual, most research in evolutionary genetics is concerned with comparisons made at the level of divergent populations or species. This is particularly true in work focused on the evolutionary genetics of natural populations. While this level of inquiry is extremely valuable, in order to develop a complete understanding of the evolutionary process we also need to understand how traits evolve within populations, on the level of differences between individuals, and in the context of natural ecological and environmental variation. A major difficulty confronting such work stems from the difficulty of assessing interindividual phenotypic variation and its sources within natural populations. This level of inquiry is, however, the main focus for many long-term field studies. Here, I take advantage of one such field study, centered on the wild baboon population of the Amboseli basin, Kenya, to investigate the possibilities for integrating functional, population, and evolutionary genetic approaches with behavioral, ecological, and environmental data. First, I describe patterns of hybridization and admixture in the Amboseli population, a potentially important component of population structure. Second, I combine field sampling, laboratory measurements of gene expression, and a computational approach to examine the possibility of using allele-specific gene expression as a tool to study functional regulatory variation in natural populations. Finally, I outline an example of how these and other methods can be used to understand the relationship between genetic variation and naturally occurring infection by a malaria-like parasite, Hepatocystis, also in the Amboseli baboons. The results of this work emphasize that developing genetic approaches for nonmodel genetic systems is becoming increasingly feasible, thus opening the door to pursuing such studies in behavioral and ecological model systems that provide a broader framework for genetic results. Integrating behavioral, ecological, and genetic perspectives will allow us to better appreciate the interplay between these different factors, and thus achieve a better understanding of the raw material upon which selection acts.

Environmental factors are a crucial determinant of an animals fitness. The effects of environment on fitness are often mediated by behavioral mechanisms as well as mechanisms that are ‘under the skin,’ such as growth and physiology. In my dissertation work, I study how two environmental factors – dominance rank and early-life conditions – are associated with growth and physiology. My colleagues and I test these links in a population of wild baboons studied by the Amboseli Baboon Research Project. The Amboseli Baboons Research Project has been collecting behavioral and demographic data on the Amboseli baboons for over 50 years, fecal hormone data for over 20 years, and blood samples collected via brief anaesthetizations for nearly 10 years. We complemented these remarkable datasets with cross-sectional data of female baboon body size.

In Chapter 1, we address two gaps in our understand of female dominance rank: (1) do higher-ranking females experience fewer stressors than lower-ranking females, and (2) how should we best quantify female dominance rank? Using fecal glucocorticoid concentrations as a proxy for the intensity and/or frequency of stressors that a baboon experiences, we find that, indeed, higher-ranking females do experience fewer stressors than lower-ranking females. Surprisingly, we also find that the best way to understand this effect is by categorizing females into two groups: alpha females, who are the highest-ranking female in the group, and everyone else.

In Chapter 2, we then focus on differences in the competitive landscapes assumed by two common measures of dominance rank, ordinal and proportional ranks. We complement theoretical work with re-analysis of 20 prior Amboseli baboon studies to show that for males, ordinal rank (i.e., number of individual ranking above the focal animal) was always a better predictor of traits than proportional rank, whereas for females, some traits were better predicted by ordinal rank, and some were better predicted by proportional rank (i.e., proportion of the group that a focal animal dominates). Our results suggest that males compete for density-dependent resources, whereas females compete for a mix of density-dependent and density-independent resources. In addition, our study demonstrates a new way to learn about the nature of within-group competition.

In Chapter 3, we present two new methods to use with body size data collected via parallel-laser photogrammetry. One of these methods was developed by colleagues here at Duke University, and the other method was developed by colleagues at George Washington University. These methods automate part of the hand-measurement process – measuring the distance between the lasers – and effectively saves time while increasing accuracy and precision of the final body size measurement. Our two methods have different strengths and weaknesses, and we anticipate that researchers will gravitate toward one or the other depending on their dataset, with the ultimate goal of increasing the use, ease, and accuracy of parallel-laser photogrammetry in studies of behavioral ecology.

In Chapters 4, we use the method developed in Chapter 3 to test whether early-life adversity stunts body size in female baboons. While this effect has been found in humans and some nonhuman animals, data on inter-individual differences in body size are extremely rare in wild primates. Using a dataset of over 2,000 images of 127 female baboons, we present the first cross-sectional growth curve of wild female baboons from juvenescence throughout adulthood. We then test whether females exposed to three main sources of early-life adversity - drought, maternal loss, or a cumulative measure of adversity – are smaller for their age in juvenescence or adulthood. We find that early-life drought predicts smaller limb length but not smaller torso length; our other measures of early-life adversity do not predict differences in body size. Our results suggest that baboons grow plastically in response to energetic early-life stress, but that this plasticity seems limited to limb growth, not torso growth.

Finally, in Chapter 5, we test a component of the biological embedding hypothesis, which predicts that early-life adversity is associated with elevated baseline inflammation as well as heightened acute inflammation in adulthood. To our knowledge, these predictions have only been tested in humans. Using serum samples collected from 89 baboons via brief anaesthetization, we measured several biomarkers of baseline and acute inflammation: c-reactive protein, soluble urokinase plasminogen activator receptor, interleukin 6, interleukin 1-beta, and tumor necrosis factor alpha. We test two measures of early-life adversity: maternal loss and a cumulative measure that incorporates 5 different potential sources of adversity. In contrast to the predictions of the biological embedding hypothesis, we find that baboons who experienced early-life adversity have a mix of comparable or lower levels of baseline and acute inflammation compared to baboons who experience no adversity. Prior tests of the biological embedding hypothesis were performed in humans who generally had access to more calories, less active lifestyles, and lower pathogen burden than wild baboons. Our results highlight the varied effects that early-life adversity can have on an organism’s development depending on the broader environment in which that organism lives.

Understanding the genetic and environmental forces that contribute to phenotypic variation is a major goal of evolutionary biology. However, social living blurs the distinction between genes and environments because the social environment is (at least in part) determined by the genes of its members. Therefore, the genes that influence an individual’s phenotype are not limited to his own genes (direct genetic effects) but potentially include the genes of individuals in his social context (indirect genetic effects).

Indirect genetic effects are thought to be of particular importance in the evolution of social behavior. Social living is a common phenotype in many animal taxa and is especially well-developed in non-human primates and humans. Social living is believed to be an adaptive response to ecological pressures and indeed, positive correlations between social behaviors and fitness components have been demonstrated in multiple species. However, despite a long-history of theoretical studies investigating the evolution of social behavior, whether social behaviors demonstrate the additive genetic variation necessary for evolution to occur remains poorly understood. No doubt this is due in part to the difficulty of determining the genetic basis of social behavior; social phenotypes are complex and by definition involve interactions between multiple individuals. Genetic variation for social behaviors, therefore, likely results from both direct and indirect genetic effects.

Here, I investigated the direct and indirect sources of additive genetic variance in both agonistic and affiliative social behaviors, in a population of wild baboons. In this population (as well as in other populations and species), affiliative social behaviors have been clearly linked to survival, an important fitness component. Therefore, I began with an investigation of the sources of variance in female fitness in our population (Chapter 2). I found that heterogeneity in female quality was a primary driver of the relationship between life history traits, and phenotypic tradeoffs between these traits were apparent only when considering variation in individual quality.

In chapter 3, I used a quantitative genetic approach to examine the direct and indirect sources of genetic variation in affiliative social behavior (grooming). I found that both grooming given and grooming received were heritable, and documented a positive genetic correlation between these traits. In chapter 4, I examined the sources of genetic variation in agonistic behavior. This investigation was complicated by the non-genetic transmission of dominance ranks from mothers to daughters. I implemented a novel method to partition social and genetic sources of similarity between relatives and found important roles for both genetic and social variance in the relationship between agonism given and agonism received.

The deleterious effects of inbreeding have been well-documented in both captive and wild populations. Mechanisms of inbreeding avoidance such as mate choice and sex-biased dispersal have also been documented across a variety of taxa. However, studies of inbreeding avoidance via mate choice are surprisingly scarce, and those that explicitly compare maternal and paternal kin are entirely absent in mammals. Here, we provide the first study to assess how behavioral inbreeding avoidance varies across kin classes in a population of wild baboons. We first examine the series of isolating barriers that prevent inbreeding, including death, dispersal, and mate choice, and we next use pedigree data to assess how behavioral inbreeding avoidance varies across kin classes. We found that while the demographic barriers of death and male-biased dispersal are extremely effective in limiting inbreeding in this population, we still found strong evidence for inbreeding avoidance via mate choice. In particular, while most kin classes exhibited inbreeding avoidance, maternal kin (mother-son pairs, maternal siblings) were more avoidant than paternal kin (father-daughter pairs, paternal siblings) despite having identical coefficients of relatedness. Finally, by taking advantage of a natural experiment in our study population, we also found that social groups with reduced sex-biased dispersal and reduced inbreeding avoidance via mate choice produced ten times as many inbred offspring.

Sexual selection has long been accepted as a widespread force of evolution shaping male traits across taxa. In recent years, biologists have begun to investigate the extent to which sexual selection may also shape traits among females. However, current models of sexual selection have largely been developed using assumptions that--while generally met in males--often do not apply to females. Thus, attempts to apply these contemporary models to the study of sexual selection in females reveal weaknesses in the theoretical framework for sexual selection research. One consequence of this for empirical research is that researchers often infer the action of sexual selection upon evidence of male mate choice. Although male mate choice is increasingly common, it is much less likely to exert selection pressure than its female counterpart. I begin by proposing a conceptual framework that explicitly accounts for ...Next, I investigate a female trait that has recently become an iconic example of sexual selection in females; that is the exaggerated estrous swellings of cercopithecine primates. By combining morphological data collected with a non-invasive photographic method and observational behavioral data with longitudinal ecological and demographic data from the ongoing Amboseli Baboon Research Project, I examine the sources of variance in this exaggerated signal of fertility. Finally, I test the hypothesis that male baboons prefer females with larger sexual swellings because those females have higher fitness. I find no evidence to support this hypothesis. Instead, my results suggest that mate choice among male baboons has evolved to detect, not the intrinsic quality of the female as has typically been proposed, but the quality of a reproductive opportunity.

Abstract If any animal is to reproduce, it must first survive to adulthood. It must navigate a veritable gauntlet as it develops first from a single-celled embryo to an immature animal living outside of its egg or mother, then through a growth phase of sexual immaturity before finally reaching adulthood. The nature and duration of these life stages varies greatly across species, but the period of an animal’s life prior to attaining sexual maturity is universally one of great vulnerability. The risks faced by immature individuals are numerous, and the determinants of survival are multi-faceted and often difficult to observe and measure. As a result, the task of understanding all the factors contributing to offspring survival in a single species may seem hopelessly challenging, even in a relatively well-studied model organism living under controlled conditions. This challenge is even greater when considering free-living animals that are subject to neither invasive monitoring, experimental manipulation, nor human protection from the environment.

The goal of this dissertation is to bring us closer to that lofty target by providing insight into the role that the social environment plays in immature survival in populations of wild mammals. In it, I place a particular emphasis on social determinants of immature development, behavior, and survival in the wild baboons of the Amboseli basin.The Amboseli baboons have been under continuous, near-daily observation since 1971. For five decades, researchers have collected a wealth of high-quality demographic, environmental, and behavioral data from over 1700 live-born individuals, as well as data from nearly 300 failed pregnancies. This extraordinary dataset has allowed me to explore a wide range of questions focused on offspring survival and phenotype in early life, before and after birth. This historical data has been my primary tool in seeking to understand how social factors affect offspring survival, but I have also used the infrastructure of the long-term study to collect my own short-term, targeted data regarding maternal care and infant social development in early life. My goal is always to link my behavioral and life history results to a broader understanding of social evolution. To this end, I have also used theory and computer modelling, in parallel with empirical approaches, to make predictions about the evolution of various social behaviors.

The results of this dissertation can be distilled into four main conclusions. First, immature baboon survival is threatened by sexually selected feticide and infanticide by males. I document this behavior by relying on demographic data, rather than observing the killing of fetuses and infants directly—an example of the power of long-term demographic data to reveal otherwise hidden social phenomena. Second, sexually selected feticide and the Bruce effect (collectively dubbed “male-mediated prenatal loss”) may be more widespread across mammalian taxa and more influential in the evolution of mammalian social behavior than is sexually selected infanticide. Yet, these phenomena have not been as thoroughly studied as has infanticide because of the difficulty in documenting them.

Third, baboon mothers influence their offspring’s phenotype in numerous ways, including their offspring’s social development, survival, and ability to successfully rear their own future offspring. As a result, maternal death that occurs early in life has previously undocumented acute and chronic effects on offspring survival such that (i) offspring are more likely to die during the juvenile period if their mothers are going to die in the near future, and (ii) the effects of early maternal loss cascade from one generation to the next, resulting in an intergenerational effect of early maternal loss on offspring survival. These effects are not restricted to baboons, but are replicated in several other primate species. These links between maternal survival and offspring fitness outcomes have important implications for the evolution of slow primate life histories: in species where stronger links exist between maternal survival and offspring fitness, there may be increased selection for longevity at the expense of fertility, leading to the evolution of slower life histories in species with extended dependence between offspring and mother that lasts well beyond the age at weaning.

Finally, I show that the intergenerational effects of early-life adversity might be mitigated by social relationships between adult males and offspring born to compromised mothers. Offspring whose mothers experienced higher levels of early adversity spend time in close proximity to relatively many adult males in their earliest months of life, and males in turn allow infants increased independence and social exploration. Collectively, the contents of this dissertation bring us several steps closer to the goal of understanding the many social determinants that influence immature development, behavior, and survival in wild primates.

Abstract

Risky foraging is a male reproductive tactic in most polygynous mammals. It is speculated to result from intense intra-sexual reproductive competition. Consequently this behavior has been speculated to increase a male's reproductive competitiveness. However, individual males may differ in their propensity to take foraging risks.

We therefore conducted a study on crop raiding behavior (a risky foraging strategy) in African elephants from the greater Amboseli ecosystem, in southern Kenya. We specifically examined the population sizes, gender and patterns of raiding elephants and investigated the effect of crop-raiding and genetic heterozygosity on male body size. We also examined the influence of age and genetic relatedness on observed patterns of association. Finally, we examined the role of life history milestones, association patterns and social structure on the acquisition of crop raiding behavior among wild free ranging male African elephants. With regard to the influence of association patterns on crop raiding behavior, we were specifically interested in understanding the mechanisms by which social learning might occur among male elephants.

Our results showed that 241elephants from different populations in the ecosystem converged to raid farms. Approximately 35% of raiders were from Amboseli National Park, and the rest were other populations in the ecosystem. We observed only post-pubertal males but not females to raid. About one third of post-pubertal males from the Amboseli population were raiders. We found evidence of habitual raiding by some individuals. Crop raiding predicted post-pubertal male size, with raiders being larger than non-raiders. This result suggests that taking risks pays off for males. Our results also showed that other variables known to influence growth like genetic heterozygosity had no effect on size-for-age in male elephants, because low-heterozygosity males were rare. The probability that an individual male is a crop raider was greater for older individuals than young males. The probability that a male is a raider was greater when his two closest associates were raiders versus when they were not raiders and when a male's second closest associate was older, versus when his second closest associate was of similar age or younger. These results suggest that increasing energetic demands associated with life history milestones and social learning play a significant role in the initiation of crop raiding behavior. Raiders did not cluster into separate social units from non-raiders, probably due to the nature of social learning exhibited by this species and due to the diffuse nature of male elephant social units.

These results have implications for understanding the evolution of risky foraging behavior in males, and for understanding the role of kin selection, dominance hierarchies and social learning in male elephant social systems. Results also have implications for understanding the spread of adaptive complex behavior in natural populations.

As global change pushes ecosystems past climate tipping points, southern African savannas will experience more heat waves and droughts. These ecosystems are home to 90% of the world’s large herbivore diversity, millions of livestock, and a rapidly growing human population expected to reach 2 billion by 2040. As a unique vestige of large Pleistocene-era herbivores and a burgeoning powerhouse of global population, it is necessary to understand how African savanna ecological communities will respond to global change. Especially concerning for these communities are increased heat loads that may overwhelm ungulate thermoregulatory systems; more frequent droughts that may dry up key surface water resources; and the expansion of veterinary fencing across the landscape, which currently restricts historic great migrations of millions of ungulates. Large herbivores regulate nutrient cycling and vegetation structure on African savannas in a way that cannot be replaced by smaller herbivores or livestock; therefore, their responses to these threats are of utmost importance to preserving savanna functioning for the future.

This dissertation addresses the effects of increasing heat, drought, and fencing on savanna ungulate communities from the individual to the metapopulation scale. In Kruger National Park, South Africa, we first address large-scale and long-term questions of drought impacts on rare antelope populations in the context of the full suite of large herbivores in the Kruger Park. We use forty years of harmonized aerial census data and a Bayesian Generalized Joint Attribute Model to understand how drought, and its interaction with other environmental covariates, drives herbivore community structure and rare antelope survival. In Khaudum National Park, Namibia, we then use a four-year dataset of 33 antelope fitted with GPS collars to answer questions on heat and fencing-induced behavioral changes on two species on opposite sides of a water-dependence spectrum. We investigate how these species differ in their reliance on surface water, cool microclimates, and shifting activity budgets when responding to higher temperatures. We then explore how they differ in their responses to veterinary fencing, and how these responses change seasonally. As climate change brings more drought and hotter temperatures to southern Africa, the findings of this dissertation indicate that the placement of artificial waterholes on the landscape will be key to rare antelope survival in the Kruger Park; that water dependence is a key factor in antelope responses to heat and fencing; and that the expression of thermoregulatory strategies for two savanna ungulates will intensify under higher temperatures. This dissertation adds these unique findings to the canon of savanna movement and fence ecology literature, and provides multiple points from which future research in this arena can improve on our expectations of savanna ungulate behavioral shifts under climate change.