An Investigation of the Relationship between Early Life Adversity and Skeletal Phenotypic Variations in Wild Amboseli Baboons
Open Access DepositedDevelopmental plasticity, the variation of phenotypes produced from a single genotype in response to environmental conditions, is a contributor to phenotypic variation and may have long-term evolutionary significance. However, the degree to which developmental plasticity in response to early life adversity has contributed to variation in the human fossil record remains poorly understood. This dissertation used a well- documented nonhuman primate population of wild savanna baboons (Papio cynocephalus) from the Amboseli Basin of southern Kenya, for whom associated behavioral and climatic data are available, to better understand the relationships between skeletal limb lengths, bone strength, and bone porosity and key environmental factors hypothesized to influence skeletal development, such as rainfall and maternal dominance rank. This population has experienced significant inter-annual variability in climate, including several severe droughts over the last three decades.Bone is a complex and highly dynamic tissue that fulfills many functions (e.g., bears mechanical load, reservoir for nutrients) and is influenced by many factors (i.e., ontogeny, biomechanics, and the environment) that are recorded at different structural levels in bone. Recognizing this complexity, bones can act as a window into an individual’s developmental past, providing insight into how the skeleton responds to the environment throughout life. Using a Bayesian mixed-effect linear ‘animal’ model with Markov Chain Monte Carlo techniques, this study examined the effect of rainfall during gestation and the first year of life, and maternal dominance rank at conception and at birth on aspects of bone growth, development, and strength in the humerus, radius, femur, and tibia in Chapters 2 and 3. In Chapter 2, the analyses focused on the cranial capacity (n = 26) and bone length [humerus (n = 34), radius (n = 35), femur (n = 36), and tibia (n = 35)]. Results in Chapter 2 indicate that neither rainfall during gestation and the first year of life nor maternal dominance rank at conception and birth have a discernible effect on bone growth and development (i.e., bone length) from early life through to adulthood. Rainfall during gestation and maternal dominance rank at conception did not appear to affect bone strength throughout ontogeny or adulthood, with the exception of the radius. Specifically, the maternal dominance rank at conception was predicted to influence bone strength in the radius, with a lower rank positively affecting bone strength. However, it appears that the infants in the sample were driving this effect. I am cautious in interpreting the results for the radius, as the infant subset of the sample is disproportionately composed of offspring from higher-ranked mothers, potentially skewing the observed effects of maternal dominance rank on bone strength. In Chapter 3, measures of bone strength were analyzed: humerus (n = 25 gestation model; n = 23 first year of life model), radius (n = 23; n =20), femur (n = 26; n = 24), and tibia (n = 25; n = 23). Rainfall during the first year of life is predicted to significantly influence some geometric properties of bone strength throughout life, specifically in the humerus and tibia. These results suggest that an increase in rainfall during the first year of life was associated with a decrease in strength. Again, the results appear to be driven by the infants in the humerus sample and when removed the predicted significance disappears. When infants were excluded, the effect of rainfall on the tibia remained significant, suggesting that rainfall during the first year of life may affect tibial bone strength throughout life. Due to increased food availability in the environment and reduced travel to obtain food, bone geometric properties of baboons may be negatively impacted by increased rainfall. Maternal dominance rank at birth is predicted to significantly influence some geometric properties of bone strength throughout life in the radius and tibia. Specifically, the results suggest that a low maternal dominance rank at birth is associated with an increase in some bone strength properties for the radius and the tibia. In Chapter 4, the case study examining two pairs of female baboons—an age- matched juvenile pair and a pair of similarly aged, but not aged-matched adult female baboons—who experienced different maternal dominance ranks during early life, found differences in the bone macro- and micro-structures. In the juvenile pair the higher- ranking baboon exhibited slightly higher porosity values in both the femur and tibia compared to the lower-ranking baboon. The higher ranking baboon bones also showed greater overall bone strength, with larger total and cortical areas, higher percent cortical area, and improved cross-sectional geometric properties, suggesting a compensatory mechanism to maintain bone strength despite higher porosity. In the adult pair, a similar pattern was observed. The higher-ranked baboon exhibited stronger bone properties compared to the lower-ranked baboon, who had higher porosity and lower geometric property values in the femur, indicating reduced resistance to mechanical forces. These differences potentially underscore the long-term effects of early life conditions, such as maternal rank and nutritional intake, on bone health. This study faced limitations, including a small, opportunistic sample size and bias in environmental exposures. Sample sizes varied across chapters and skeletal elements, with some bones having larger sample sizes than others. Over 90% of the baboons in the sample experienced low rainfall or drought conditions, and 55% were from higher-ranking mothers, limiting generalizability. Additionally, genetic relatedness among individuals (31% from the same social group) introduced potential confounding effects, despite accounting for this in prediction models. These limitations, along with challenges in accounting for sexual dimorphism due to the small sample size, complicate the ability to disentangle genetic and environmental effects. For these reasons, the results described herein should be interpreted with caution. However, the results provide valuable insights into early life environmental impacts on bone development, offering a framework for future research with expanded datasets. This dissertation advances understanding of early life environments and their impact on skeletal development, with broader implications for interpreting phenotypic variation in fossil and bioarchaeological contexts. This international collaboration also supported training and mentorship of undergraduate and early-stage graduate students, including individuals from underrepresented backgrounds.
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