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Duke University Dissertation Template Lemur Teeth in Three Keys: Dietary Adaptation, Ecospace Occupation, and Macroevolutionary Dynamics by Ethan L. Fulwood Department of Evolutionary Anthropology Duke University Date:_______________________ Approved: ___________________________ Doug Boyer, Supervisor ___________________________ Richard Kay, Chair ___________________________ Daniel McShea ___________________________ Blythe Williams ___________________________ Elizabeth St. Clair Dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Evolutionary Anthropology in the Graduate School of Duke University 2019 ABSTRACT iv Lemur Teeth in Three Keys: Dietary Adaptation, Ecospace Occupation, and Macroevolutionary Dynamics by Ethan Fulwood Department of Evolutionary Anthropology Duke University Date:_______________________ Approved: ___________________________ Doug Boyer, Supervisor ___________________________ Richard Kay, Chair ___________________________ Daniel McShea ___________________________ Blythe Williams ___________________________ Elizabeth St. Clair An abstract of a dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Evolutionary Anthropology in the Graduate School of Duke University 2019 Copyright by Ethan Fulwood 2019 Abstract Dietary adaptation appears to have driven many aspects of the high-level diversification of primates. Dental topography metrics provide a means of quantifying morphological correlates of dietary adaptation and can be used to reconstruct dietary adaptation in extinct taxa, model ecospace occupation, and capture macroevolutionary trends across deep time. However, difficulties may arise in the interpretation of dental topography metrics from A) their sensitivity to digital mesh processing choices; B) their tendency to average morphological information across tooth surfaces; and C) potential mismatches between the material properties understood theoretically to drive tooth shape and the measured properties of categorically defined primate diets. The full potential of pairing dental topography metrics with modern phylogenetic comparative methods, which would allow the evolutionary history of diet in large clades to be explored statistically, has yet to be explored. In this dissertation, I attempt to address issues in the application of dental topography metrics, and extend them to new questions, using strepsirrhine primates as a model. The effectiveness of a recently described dental topography metric, ariaDNE, which is robust to details of mesh processing, in describing dietary adaptation in lower second molars is assessed. It is found that it performs at least as well as metrics more sensitive to mesh processing decisions. ariaDNE is then applied to segmented regions of iv lower second molars in order to assess the effect of averaging together potentially adaptively distinct tooth structures. I found no evidence that the aggregation of tooth structures significantly impairs dietary classification. These studies employ explicit methods for measuring overfitting risk, which has not previously been emphasized in applications of dental topography metrics. Tooth shape is believed to reflect differences in the underlying material properties of the foods consumed by mammals, but the categories used to classify taxa to diets have inconsistent relationships with these food material properties. I attempt to address this inconsistency by relating tooth shape to expected geographic gradients in food material properties, an approach known as ecometrics. Dry, seasonal environments are expected to be associated with dental topography metrics associated with processing tougher foods. I find that ariaDNE is highest in highly seasonal but wet environments, supporting a role for the seasonal exploitation of fallback foods and that the availability of new leaves during wet periods may be important in driving community tooth sharpness. Tooth complexity is primarily driven by a stepwise increase in rainforest environments. Dental topography metrics are then applied to several questions concerning the evolutionary history of lemurs. They are used to reconstruct the diets of seven genera of recently extinct, giant, subfossil lemurs, and find many of them to have exploited fruits and hard objects. Ecometric models are also applied to the reconstruction of v paleoclimate at the ~500 year-old subfossil cave site of Ankilitelo, which records the last appearance of many subfossil lemur taxa. Models reconstruct a moister climate for Ankilitelo at the time of the accumulation of its subfossil fauna, supporting a role for climate alteration in the extirpation of the giant lemurs. Finally, Dental topography metrics are combined with phylogenetic comparative methods to model the dietary evolution of lemurs in the context of adaptive radiation theory. Dental topography metrics do not show an early burst in rates of change or a pattern of early partitioning of subclade disparity in lemurs. However, rates of transition toward folivory were highest during the Oligocene, an interval of possible forest expansion on the island and of the dispersal of non-chiromyiform lemurs to Madagascar. Reconstruction of the ancestral molar morphology of ancestral nodes of the lemur tree suggest that the diversification of large bodied lemurs may have been driven by a shift toward the exploitation of defended plant resources. vi Dedication To my parents, Brenda and Robert Fulwood, who inspired in me a sense of curiosity, a love of nature, and a sense of place. vii Contents Abstract ......................................................................................................................................... iv List of Tables ................................................................................................................................ xii List of Figures .............................................................................................................................xiv Acknowledgements ...................................................................................................................xvi 1. Introduction ............................................................................................................................... 1 1.1 Dental ecomorphology and diet ..................................................................................... 3 1.2 Food material properties ................................................................................................. 8 1.3 Ecometrics ........................................................................................................................ 10 1.4 Disparity and modelling evolution .............................................................................. 12 1.5 Adaptive radiation ......................................................................................................... 18 1.6 Evolutionary history of the strepsirrhines .................................................................. 23 1.7 Dissertation overview .................................................................................................... 26 1.7.1 Overview .................................................................................................................... 26 1.7.2 Chapter 2..................................................................................................................... 27 1.7.3 Chapter 3..................................................................................................................... 27 1.7.4 Chapter 4..................................................................................................................... 28 2. Tooth shape and diet in strepsirrhine primates .................................................................. 29 2.1 Introduction ..................................................................................................................... 30 2.1.1 Molar shape and dietary adaptation ...................................................................... 31 2.1.2 Disaggregating adaptation in tooth surface features ........................................... 36 viii 2.1.3 Objectives .................................................................................................................... 36 2.2. Methods .......................................................................................................................... 37 2.2.1 Sample ......................................................................................................................... 37 2.2.2 Dental topography metrics ...................................................................................... 40 2.2.3 Shape segmentation .................................................................................................. 41 2.2.4 Dietary signal and dental topography metrics ..................................................... 42 2.2.5 Dietary signal in the segmented molar .................................................................. 44 2.2.6 Reconstructed dietary ecology in subfossil lemurs .............................................. 45 2.3. Results ............................................................................................................................. 47 2.3.1 Dental topography metrics and dietary category ................................................. 48 2.3.2 Whole tooth reclassification success ......................................................................
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