How the Outside Gets in: Linking Social and Physical Environments with Physiology and Body Size in Wild Baboons

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.