Dissertations, Theses, and Capstone Projects

Date of Degree

9-2020

Document Type

Dissertation

Degree Name

Ph.D.

Program

Anthropology

Advisor

Jessica Rothman

Committee Members

Larissa Swedell

Stephanie Levy

Andres Gomez

Subject Categories

Behavior and Ethology | Biological and Physical Anthropology | Comparative Nutrition | Molecular, Genetic, and Biochemical Nutrition | Other Ecology and Evolutionary Biology | Other Genetics and Genomics | Other Nutrition | Zoology

Keywords

microbiome, ecology, nutritional ecology, development, life history, metabolome, diet-microbe

Abstract

In species who consume folivorous diets, immature individuals must contend with the challenges of extracting nutrients from fibrous foods before dietary adaptations and strategies are fully developed. Additionally, immatures have distinct nutritional needs to support their stage-specific metabolic and biophysiological requirements. To meet these stage-specific needs, while constrained by underdeveloped feeding strategies and digestive capacities, immatures may adopt distinct diets better suited to their specific developmental context. However, where dietary modification is constrained by low dietary diversity or landscape homogeneity, it is unclear how immature individuals compensate through alternative strategies. In turn, little is known about the nutritional and life history implications of restrictions in alternative foraging strategies.

This dissertation is divided into three main studies. Firstly, a comprehensive literature review examines the theoretical framework and provides context for the importance and relevance of this topic to the broader study of life history patterning and developmental outcomes. Following this, the diet of mountain gorillas across development is characterized through a combination of four hour focal follows and nutritional biochemical analysis of consumed food items. The results of this study suggest that mountain gorillas self-select their diets to age- and stage-specific nutrient targets, occupying unique nutritional niches within the species’ overall nutritional landscape. To meet these age-specific nutritional needs within their relatively constrained ecological environment, immature mountain gorillas engage in three principle behavioral strategies: 1) differential reliance on food items, including increased consumption of highly digestibly foods as well as self-selection of a balance of nutrients higher in non-protein energy intake relative to protein intake, 2) compensatory foraging and increased overall foraging effort to compensate for biophysiological limitations (i.e. gut size) and behavioral limitations (feeding/foraging competency), and 3) extended use of mother’s milk as a nutritional ‘buffer’ during periods of preferred food scarcity.

Next, this dissertation considers the one of the most complex and dynamic systems involved in the regulation and utilization of nutrients: the gastrointestinal microbiome. The gastrointestinal microbiome is first characterized using a large library of mountain gorilla samples, spanning all members of three social groups. This characterization confirms previous work on the microbiome of mountain gorillas, and further establishes that the microbiome of mountain gorillas is relatively aseasonal, but can be differentiated based on age-class. Contrary to expectations of diversity, the infant mountain gorilla microbiome is broadly less diverse than those of juvenile and adult individuals, with higher abundance of key hydrogenotrophic taxa and sulfate-reducing bacteria. These taxa may play a role in preventing hydrogen accumulation in the gut during development. Additionally, this study shows that there are differences in the abundance of major phyletic groups (specifically, Actinobacteria, Firmicutes, and Bacteroidetes), suggesting that immature individuals may house microbiomes with greater capacity for energy harvest, potentially as an adaptation to maximize nutrient availability during periods of growth and development where individuals are sensitive to environmental perturbation and dietary shortfalls.

Lastly, this dissertation considers the dietary metabolome of mountain gorillas through characterization of the fecal metabolome, in a pivotal step to bridge the gap between observed diet/nutrient intake and individuals’ capacity to use ingested nutrients (including through microbiome-mediated nutrient pathways). Mountain gorillas demonstrate distinct metabolomes throughout development, especially with respect to the relative concentration of lipid and lipid-derived molecules and organic acids/phenolic compounds and their derivatives. Additionally, this study explicitly considered the potential influence of observed diet and nutrient intake as drivers of differentiation among age groups; it is found that protein intake is a primary driver of infant microbiome differentiation, and non-digestible fibers are a primary driver in differentiating both the adult microbiome and metabolome.

Through these studies, this dissertation provides the first comprehensive examination of nutritional ontogeny through a multi-layered ecological approach, by examining these complex relationships in immature mountain gorillas (Gorilla beringei). This dissertation significantly contributes to our understanding of nutritional ontogeny and compensatory nutritional strategies among great apes living at the extreme end of their known ecologies, and, in turn, provides a lens towards the potential evolutionary basis of these behaviors and adaptations.

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