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«Doctoral Committee: Professor L. Lacey Knowles, Chair Research Associate Professor Liliana Cortés Ortiz Professor Diarmaid Ó Foighil Professor John ...»

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Biotic and abiotic factors influencing diversification of herbivorous mammals


Lucy Tran

A dissertation submitted in partial fulfillment

of the requirements for the degree of

Doctor of Philosophy

(Ecology and Evolutionary Biology)

in the University of Michigan


Doctoral Committee:

Professor L. Lacey Knowles, Chair

Research Associate Professor Liliana Cortés Ortiz

Professor Diarmaid Ó Foighil

Professor John C. Mitani

© Lucy Tran


To my parents, for allowing me to follow my dreams, and to Joe, for supporting me while I pursue them ii


I am forever grateful to Lacey Knowles, Liliana Cortés Ortiz, John Mitani, Diarmaid Ó Foighil, Miriam Zelditch, Dan Rabosky, Catherine Badgley, Qixin He, Anna Papadoupoulou, and Diego Alvarado Serrano for the valuable and thought-provoking discussions of science throughout my graduate training. Miriam Zelditch, Diego Alvarado Serrano, Eladio Marquez, Elen Oneal, Raquel Marchan-Rivadeneira, and Hayley Lanier are recognized for their instrumental guidance with morphometrics for Chapter II and Carlos Anderson for troubleshooting the BAMM analyses for Chapter III. I am indebted to Anna Papadopoulou, Qixin He, Mark Christie, Pavel Klimov, Raquel Marchan-Rivadeneira, and Joseph Knoedler for their insightful comments on previous versions of the manuscripts comprising this dissertation. Thanks are also owed to the members of the Knowles lab throughout the years for the scientific enrichment, in particular John McCormack, Amanda June Zellmer, Danielle Edwards, Huateng Huang, and Tim Connallon. I cannot thank Ken Nagy, Travis Longcore, and my Spring 2006 Field Biology Quarter friends enough for introducing me to the joys of field research. Thea Wang, Kyle Larson, Corey Duberstein, and Shauna Price were inspiring research mentors and role models. I could not have completed this thesis without the sanity check provided by my friends (near or far) throughout the years, especially Linda Quach, Nancy Su, Rachel Cohen, Jenabel Lee, Qixin He, Kelsey Pressler, Jingchun Li, Leiling Tao, Gyorgy Barabas, and Michael Sheehan. You all have my deepest gratitude. Funding for this dissertation was generously provided by the Museum of iii Zoology Hinsdale and Walker Awards, EEB Block grants, Rackham International Research Award, American Society of Mammalogists Grants-in-Aid, and a National Science Foundation Graduate Research Fellowship.


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Table 2.1.

Fits of diversification models to phylogenetic data

Table 2.2.

Fits of the folivory-dependent speciation and extinction models

Table S2.1.

Landmarks and semilandmarks of mandible shape

Table S2.2.

Cranio-mandibular dental (CMD) characters

Table S2.3.

Taxonomy of colobine monkeys (subfamily Colobinae)

Table S2.4.

Diet data of species

Table S2.5.

Fits of diversification models to phylogenetic data

Table S2.6.

Fits of the folivory-dependent speciation and extinction models

Table 3.1.

Lineages of terrestrial, herbivorous mammals that were analyzed in this study..........81 Table 3.2. Phylogenetic generalized least-squares regressions

Table S3.1.

List of sources for trophic level and fermentation state of species considered in this study

Table S3.2.

List of dietary items in primate species' diets, reclassified using the PanTHERIA scheme

Table S3.3.

Description of variables used to compute the maximum environmental disparity metric

Table 4.1.

Description of variables used to calculate multivariate climate anomaly..................133 Table 4.2. Phylogenetic signal of multivariate climate anomaly and species richness...............134

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Table 4.4.

Scores from phylogenetic principal components analysis (PCA) of climate anomaly.

Table 4.5.

Species at climatic instability limits of hindgut and foregut-fermenting mammals...137 Table 4.6. Regression analyses of climate anomaly and species richness

Table S4.1.

Area under the operator receiving curve (AUC) of MaxEnt models for species analyzed in this study

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Figure 2.1.

Lineage-through-time plots of the African and Asian clades

Figure 2.2.

Disparity through time of feeding morphology

Figure 2.3.

Folivory-dependent rates of speciation and extinction

Figure S2.1.

Gamma statistics for the phylogenies

Figure S2.2.

Node height tests of feeding morphology

Figure S2.3.

Phylogeny of Colobinae

Figure 3.1.

Cladogram of 46 lineages of terrestrial, herbivorous mammals selected for comparative analyses

Figure 3.2.

Relationship between niche specialization and speciation

Figure 3.3.

Differences in niche specialization between foregut and hindgut-fermenting clades.

Figure 3.4.

Differences in speciation between foregut and hindgut-fermenting clades..............101 Figure S3.1. Scatterplot of diet breadth reclassified in this study and data from PanTHERIA for primates

Figure 4.1.

Maps of species richness

Figure 4.2.

Plot of phylogenetic principal components of climate anomaly

Figure 4.3.

Phylogenetic principal components bi-plot

Figure 4.4.

Comparisons of climate anomaly and species richness between hindgut and foregut

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Figure 4.5.

Geographic distributions of artiodactyl species at limits of climatic instability.......154 Figure 4.6. Climatic instability space of herbivorous mammals

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Both biotic and abiotic factors are known to control diversification. Though these factors are believed to operate at distinct temporal and spatial scales (i.e., the multilevel mixed model), often the scales at which key processes and outcomes of diversification operate are ambiguous or confused. To explore the dependence of factors promoting diversification on spatiotemporal scales as well as the biology and ecology of clades, my dissertation examined the interactive effects of lineage-specific traits with ecology and environment at multiple taxonomic, temporal, and spatial scales. I focused on the effects of a novel digestive strategy, foregut fermentation, in herbivorous mammals. In Chapter II, I tested predictions of a popular macroevolutionary model to evaluate the role of an abiotic factor, ecological opportunity, in the diversification of the foregut-fermenting Old World colobine monkeys. This work corroborated a growing body of work that the model is sensitive to the geographic scale of diversification, in particular to multiple dispersal-divergence events within a single radiation. In addition to the abiotic factor, I also found evidence for an important role of dietary specialization, a biotic factor, on the diversification of Asian colobines. Deviating from the current multilevel mixed model, these findings showed that both biotic and abiotic factors can be important controls on diversification at long timescales and large geographical scales. In Chapter III, I tested the effects of foregut fermentation on the relationship between ecological specialization and speciation rates in the terrestrial, herbivorous mammals. My findings indicated that foregut fermentation did mediate

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differences in speciation among clades at intermediate temporal and geographical scales. In Chapter IV, I investigated the effects of environmental change, specifically historical climatic perturbations, and its interaction with digestive strategy on speciation rates of the terrestrial, herbivorous mammals. I found that climatic instability since the Last Glacial Maximum had stronger, multifarious effects on the richness of foregut-fermenting mammals. In contrast, hindgut herbivores experienced bounded instability across the continents on which they occur.

These findings support important roles for both biotic and abiotic factors on species richness over short timescales and intermediate geographical scales. Overall, my findings from Chapters II-IV together show that not only are the effects of biotic and abiotic factors on diversity important on spatiotemporal scales not currently recognized in the multilevel mixed model, the effects of the factors themselves are likely to vary based on the biological and ecological differences found within and among clades.

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A longstanding question in evolutionary biology asks why some groups of organisms are phenomenally speciose with exceptional phenotypic diversity while others are depauperate in both aspects. Radiations span the continuum of species and phenotypic diversity, with the classic cases of adaptive radiation lying at one end with many species and morphological forms. Some groups such as the cichlids (Farias et al. 1999) are represented at both extremes of the continuum. In such cases the disparity in species and phenotypic richness among lineages sharing common ancestry implicates differing ecological and/or environmental contexts (Seehausen 2007), lineage-specific properties (Moyle et al. 2009), or the joint action of these two factors in the generation of disparate diversification outcomes.

Climatic and orographic events (Richardson et al. 2001) influence the probability of speciation and extinction by controlling the strength of gene flow between populations and the likelihood of population persistence. Furthermore, often populations encountering vacant or underutilized niches (“ecological opportunity”) (Schluter 2000) are assumed to speciate rapidly due to the lack of ecological constraints posed by competition and predation (Seehausen 2007, Yoder et al.

2010). Radiations on islands and in water bodies that were initially depauperate of species highlight the importance of ecological opportunity in promoting phenotypic and species diversity

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specific traits also potentially influence diversification (Moyle et al. 2009). This dissertation examines the interaction between lineage-specific traits, ecology, and environment on the diversification and morphological evolution of exemplar clades. I apply state-of-the-art methods in phylogenetic comparative biology, morphometrics, and species distribution modeling to address these questions at varied taxonomic, temporal, and spatial scales. I focus on the effects of a novel digestive strategy, foregut fermentation, in the herbivorous mammals. Foregut fermentation evolved independently at least four times in the marsupials, sloths, artiodactyls, and primates and at least once in birds.

Foregut fermentation may operate as a “key innovation” (Simpson 1944, 1953) that contributed to the diversification of herbivorous mammals, similar to the decoupled pharyngeal jaws (Seehausen 2006) and mouth-brooding (Salzburger et al. 2005) of African cichlid fish, subdigital toepads of anole lizards (Losos 2009), and nitrile-specifier protein in pierid butterflies (Wheat et al. 2007). Key innovations are phenotypic novelties that allow lineages to exploit new or previously inaccessible resources upon their acquisition and are commonly invoked in cases of elevated speciation rates, species richness, and/or phenotypic diversity in a broad range of organisms (e.g., Berenbaum et al. 1996, Bond and Opell 1998, Lynch 2009, Vamosi and Vamosi 2010, Rutschmann et al. 2011).

In Chapter II, I test for temporal concordance between rates of diversification and morphological evolution to evaluate the role of ecological opportunity in the foregut-fermenting colobine

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morphological evolution are high early in a radiation but decline later due to reduced niche availability (Lovette and Bermingham 1999, Phillimore and Price 2008, Burbrink and Pyron 2010, Yoder et al. 2010). In conjunction with the biogeographic history of colobines, my findings suggest that constraints arising from dietary specialization and decreasing availability of new adaptive zones over time explain temporal changes in diversification but not morphological evolution in the Asian radiation. Due to the lack of appropriate forest habitat, ecological opportunity did not play a major role in the African radiation. Lastly, I attribute departures from the early burst model to the iterative series of diversification events that follow the monkeys' dispersal to Eurasia.

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