Browsing by Subject "Primate"

Smooth pursuit eye movements are movements of the eyes that are used to foveate moving objects. Their precision and adaptation is believed to depend on a constellation of sites across the cerebellum, but only one region’s contribution is well characterized, the floccular complex. Here, I characterize the response properties of neurons in the oculomotor vermis, another major division of the oculomotor cerebellum whose role in pursuit remains unknown. I recorded Purkinje cells, the output neurons of this region, in two monkeys as they executed pursuit eye movements in response to step ramp target motion. The responses of these Purkinje cells in the oculomotor vermis were very different from responses that have been documented in the floccular complex. The simple spikes of these cells encoded movement direction in retinal, as opposed to muscle coordinates. They were less related to movement kinematics, and had smaller values of trial-by-trial correlations with pursuit speed, latency, and direction than their floccular complex counterparts. Unlike Purkinje cells in the floccular complex, simple spike firing rates in the oculomotor vermis remained unchanged over the course of pursuit adaptation, likely excluding the oculomotor vermis as a site of directional plasticity. Complex spikes of these Purkinje cells were only partially responsive to target motion, and did not fall into any clear opponent directional organization with simple spikes, as has been found in the floccular complex. In general, Purkinje cells in the oculomotor vermis were responsive to both pursuit and to saccadic eye movements, but maintained tuning for the direction of these movements along separate directions at a population level. Predictions of caudal fastigial nucleus activity, generated on the basis of our population of oculomotor vermal Purkinje cells, faithfully tracked moment-by-movement changes in pursuit kinematics. By contrast, these responses did not faithfully track moment-by-moments changes in saccade kinematics. These results suggest that the oculomotor vermis is likely to play a smaller role in influencing pursuit eye movements by comparison to the floccular complex.

There is a long-standing claim that humans and nonhuman primates share an evolutionarily ancient system of nonverbal number representation. By and large, the focus in the field has been on providing existence proofs of numerical competence in wide-ranging taxa or using individual species as models for comparisons with humans. Recent findings in numerical cognition have suggested that evidence for approximate numerical abilities in nonhuman species may indicate that humans and animals share a cognitive system for representing numerosities nonverbally. To date, little is known about the contextual and quantitative limits of that system, or how those limits differ between species. The studies presented here take a comparative, behavioral approach to characterizing species differences and similarities in the approximate number system, and the contexts that affect that system. Collectively, this set of studies provides evidence that the approximate number system evolved in primates as a malleable system in which numerical representations are accessed spontaneously and improved through training. Despite the sensitivity of the system to experience and context individual differences in sensitivity are greater than species differences suggesting that the selective pressures that constrained its evolution were early and general and that species variation in social group size and diet have less influence on the ANS. Finally my studies indicate that the ANS supports approximate arithmetic and is consistent with the idea that ANS representations evolved to allow animals to calculate the world around them.

The inferior colliculus (IC) is an auditory midbrain nucleus essential to the perception of sound frequency and the localization of sound source; yet it remains unclear how the firing rate of primate IC neurons contribute to the localization of concurrent sounds of variable sound frequencies. In this work, I extracellularly recorded the activity of 105 IC neurons while two adult macaque monkeys reported the location(s) of either a single bandpass filtered sound or two concurrent bandpass filtered sounds spatially separated by 24° and separated in sound frequency by 0.25 - 2 octaves. Monkeys performed this task well, with an accuracy of about 80% on single sound trials and about 90% on dual sound trials. The improvement in performance on dual sound trials was not explained by dual sound modulations of IC neural response functions. On dual sound trials, IC neuron receptive fields broadened, and sound frequency accounted for less variance in the dual sound response; and these changes decreased the performance of a maximum-likelihood decoder in correctly labeling the condition of a held out dual sound trial by about 20%. Overall, these results suggest that changes to the IC neural response functions elicited by the presence of a second, concurrent, sound should impair rather than facilitate the IC encoding of concurrent sounds and that an alternative explanation is required to account for monkey performance. I next investigated if recently discovered response alternations, suggested to underlie the encoding of concurrent sounds, were present in the recorded populations. These response alternations occur when an IC neuron alternates its firing rate between the rate corresponding to each component sound of a dual sound pair. These response alternations were observed in about 60% of IC neurons and their contribution to the population response remained stable across the full, 2 octave, range of frequency separations tested. Thus, response alternations are a general mechanism used by the IC to potentially facilitate the encoding of multiple sounds and these results add to a growing body of work observing response alternations across brain areas. The measurements I performed clearly indicate that neurons in the primate IC are sensitive to not only sound frequency and location but also the number of sounds in the environment. Future empirical and theoretical work is needed to elucidate how exactly these response alternations arise and are read out by downstream neurons to allow for the perception of concurrent sounds.

Reconstructing locomotor patterns from fossils is crucial for understanding the origins of primates and important transitions in various primate clades. Recent studies suggest that the semicircular canals of the inner ear provide evidence about locomotion. The canals sense rotational head accelerations and drive reflexes essential for normal movement. Because bony aspects of canal morphology influence canal sensitivity, this system can be studied in osteologic specimens and fossils. Variation in canal morphology in living and, by inference, extinct primates has been attributed to interspecific differences in locomotor behavior. However, the manner in which movement selects for canal morphology is debated, alternative scenarios are plausible, and no relevant measurements are available documenting head movements in primates.

To refine proposed links between canal morphology and locomotor function, and to resolve conflicting functional interpretations, this study examines head rotations in lemurs and lorises exhibiting diverse locomotor behaviors. Three-dimensional kinematic analyses were used to characterize angular velocities of the head during locomotion. These data are used to test hypotheses concerning intraspecific, interspecific, and body-size dependent variation in head rotations. Cranial CT scans are used to model canal sensitivity to rotations in different directions. Observed patterns of head rotation are compared to predicted patterns of sensitivity to test hypotheses about the relationship between locomotor behavior and canal design.

Evaluation of existing locomotor inferences reveals that brain size exerts a significant effect on canal size and that the prevailing equations for predicting agility from body and canal size are highly inaccurate. Intraspecific comparisons between maps of observed angular velocity and predicted sensitivity allow identification of map types associated with different general locomotor modes and do not support existing hypotheses about the primary selective forces acting on canal morphology. The new data are used to formulate and test a novel "fast-accurate hypothesis" to explain why all vertebrates are more sensitive to rotations about some axes than others. The fast-accurate hypothesis stipulates that angular velocities presented about axes of mean sensitivity are most accurately interpreted by the brain, and that selection aligns axes of mean sensitivity with axes of habitually fast rotation because accurate perception of rapid rotations confers survival benefit. The fast-accurate hypothesis was used to predict which features of the canals should be correlated with high mean angular velocities of head movement. Novel equations that predict behavior from these newly identified canal morphologies were generated and found to outperform existing equations when tested on the original sample of 11 strepsirrhine species.

The ability to monitor, learn from, and respond to social information is essential for many highly social animals, including humans. Deficits to this capacity are associated with numerous psychopathologies, including autism spectrum disorders, social anxiety disorder, and schizophrenia. To understand the neural mechanisms supporting social information seeking behavior requires understanding this behavior in its natural context, and presenting animals with species-appropriate stimuli that will elicit the behavior in the laboratory. In this dissertation, I describe a novel behavioral paradigm I developed for investigating social information seeking behavior in rhesus macaques in a laboratory setting, with the use of naturalistic videos of freely-behaving conspecifics as stimuli. I recorded neural activity in the orbitofrontal and lateral prefrontal cortex of monkeys as they engaged in this task, and found evidence for a rich but sparse representation of natural behaviors in both areas, particularly in the orbitofrontal cortex. This sparse encoding of conspecifics' behaviors represents the raw material for social information foraging decisions.

Deciphering the molecular mechanisms driving the phenotypic differences between humans and primates remains a daunting challenge. Mutations found in protein coding DNA alone has not been able to explain these phenotypic differences. The hypothesis that mutations in non-coding regulatory DNA are responsible for altered gene expression leading to these phenotypic changes has now been widely supported by differential gene expression experiments. Yet, comprehensive identification of all regulatory DNA elements across different species has not been performed. To identify the genetic source of regulatory change, genome-wide DNaseI hypersensitivity assays, marking all types of active gene regulatory element sites, were performed in human, chimpanzee, macaque, orangutan, and mouse. Many DNaseI hypersensitive (DHS) sites were conserved among all 5 species, but we also identified hundreds of novel human- and chimpanzee-specific DHS gains and losses that showed signatures of positive selection. Species-specific DHS gains were enriched in distal non-coding regions, associated with active histone modifications, and positively correlated with increased expression - indicating that these are likely to be functioning as enhancers. Comparison to mouse DHS data indicate that human or chimpanzee DHS gains are likely to have been a result of single events that occurred primarily on the human- or chimpanzee-specific branch, respectively. In contrast, DHS losses are associated with events that occurred on multiple branches. At least one mechanism contributing to DHS gains and losses are species-specific variants that lead to sequence changes at transcription factor binding motifs, affecting the binding of TFs such as AP1. These variants were functionally verified by DNase footprinting and ChIP-qPCR analyses.

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.

The composition and function of mammalian gut microbiomes are shaped by complex endogenous and exogenous factors that present on evolutionary and proximate timescales. In the Anthropocene era, host-associated microbiota are inevitably, yet differentially, influenced by natural and anthropogenic factors that vary across individuals and populations. In this dissertation, I used descriptive and experimental approaches, largely within a single species, the ring-tailed lemur (Lemur catta), to probe the roles of host physiology, environmental conditions, anthropogenic perturbation, and microbial environment in shaping primate microbiota across scales. First, I conducted a broad investigation of ring-tailed lemur gut microbiota and soil microbiota across 13 lemur populations (n = 209 individuals) spanning this species’ natural range in Madagascar, as well as multiple captivity settings in Madagascar and the U.S. By analyzing the lemur and soil microbiota, I showed that lemur gut microbiota vary widely within and between wild and captive populations, and that lemur and soil microbiota covary, suggesting a role for environmental acquisition in shaping interpopulation variation. Second, I analyzed vaginal, labial, and axillary microbiota of female ring-tailed lemurs and Coquerel’s sifakas (Propithecus coquereli) at the Duke Lemur Center (DLC) to demonstrate the influences of stable traits (e.g., species identity and mating system) and transient traits (e.g., ovarian hormones and forest access). We found that the effects of transient traits build on underlying differences mediated by stable traits. Third, and further focusing on DLC lemurs, but with a concentration on anthropogenic influence, I worked with a team of researchers to perform an experimental manipulation in ring-tailed lemurs to determine the influence of antibiotic treatment, with or without subsequent fecal transfaunation, on lemur gut microbiomes. I applied ecological frameworks to show that different facets of lemur microbial communities, such as bacterial diversity and composition, followed different recovery trajectories following antibiotic treatment. Fourth, I expanded my focus back to multiple ring-tailed lemur populations in natural and captivity settings to investigate the links between anthropogenic disturbance and antibiotic resistance genes (ARGs). I analyzed ARGs in wild and captive lemurs and soil from their habitats to show that lemur ARGs were correlated with anthropogenic disturbance and covaried with soil ARGs; lemur resistomes reflects multiple routes of ARG enrichment, including via antibiotic treatment or environmental acquisition. Integrating across these four data chapters, my results reveal that (a) the foundations of lemur-associated microbiomes are structured according to broad environmental conditions (e.g., wild vs. captive populations), but that between and within these broad categories, lemur microbiota are sensitive to more nuanced environmental variation, (b) lemur microbiota and resistomes co-vary with environmental microbiota, demonstrating the potential role of environmental acquisition in shaping host-associated communities across varying environments, and (c) integrating host microbial data across scales (e.g., at the individual and population level) with data on multiple facets of microbial communities (e.g., diversity, composition, membership, and resistomes), was key to providing a holistic perspective on host-associated and environmental microbe interactions across different microbial landscapes.

Because water is essential for life, when it is scarce, it may be one of the most important drivers of animal behavior. Despite its clear importance, water is relatively poorly studied in terms of its impact on primate behavior, and previous research has been limited to observational studies. This dissertation takes a combined experimental and observational approach to study behavior related to water acquisition in captive and wild lemurs. Specifically, I investigated how several dimensions of water sources influence lemur behavior, including their parasite transmission risk, spatial distribution, and predation risk. In experiments, I manipulated the fecal contamination of water with several species of lemurs in captivity at the Duke Lemur Center, and found that lemurs strongly preferred clean to feces-contaminated water in captivity (Chapter 2). I expanded this initial study to a more comprehensive examination of the impact of water scarcity on the behavior of wild red-fronted lemurs (Eulemur rufifrons) in Kirindy Forest, Madagascar. This wild study population requires drinking water to survive, but water is extremely limited during the dry season. I experimentally manipulated water availability in the habitat by introducing artificial water sources, and I tracked how changes to the distribution of water influenced the ranging patterns of the lemurs recorded by GPS collars. Lemur groups shifted the intensity of their habitat use relative to natural and experimental water availability (Chapter 3). Using a similar experimental approach to the study in captivity, I determined that wild, water-limited lemurs also preferred to drink clean water. Based on lemur groups’ selection of natural water sources as measured with camera traps, wild lemurs also selected water sources with lower fecal contamination more frequently, but with some constraints. Lemurs were more likely to return to waterholes and returned to them after shorter time intervals when they had lower levels of fecal contamination in the areas around them. However, lemurs’ natural waterhole choices reflected that fecal contamination was a secondary factor determining water source selection, behind travel distance (Chapter 4). Finally, I examined how predation risk, i.e. the presence of fossa (Cryptoprocta ferox) and Madagascar harrier hawks (Polyboroides radiatus), influenced red-fronted lemurs’ spatiotemporal patterns of waterhole use. Red-fronted lemurs used waterholes at times of day when predators were least likely to be present (Chapter 5). This study, with its combined experimental and observational approach, identifies water as an important factor that shapes wild primate behavior. I found that lemurs were flexible in their responses to changes in water distribution, parasite risk, and predation risk. I suggest that water should be the focus of future behavioral research in primates, especially given the relevance of water for human evolution and the potential for climate change and human land use to further alter water availability.