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Selection and Plasticity: Novel Phenotypic Trajectories in the Era of Climate Change

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Selection and Plasticity: Novel Phenotypic Trajectories in the Era of Climate Change Selection and Plasticity: Novel Phenotypic Trajectories in the Era of Climate Change A dissertation presented to the faculty of the College of Arts and Sciences of Ohio University In partial fulfillment of the requirements for the degree Doctor of Philosophy Anthony L. Gilbert May 2020 © 2020 Anthony L. Gilbert. All Rights Reserved. 2 This dissertation titled Selection and Plasticity: Novel Phenotypic Trajectories in the Era of Climate Change by ANTHONY L. GILBERT has been approved for the Department of Biological Sciences and the College of Arts and Sciences by Donald B. Miles Professor of Biological Sciences Florenz Plassmann Dean, College of Arts and Sciences 3 ABSTRACT GILBERT, ANTHONY L., Ph.D., May 2020, Biological Sciences Selection and Plasticity: Novel Phenotypic Trajectories in the Era of Climate Change Director of Dissertation: Donald B. Miles Rising temperatures across the planet are exposing populations to environmental conditions previously unexperienced by these lineages, and the responses to these changes are myriad. Depending on the species and population, responses to changing climates can encompass shifts in geographic ranges, rapid genetic adaptation, or new phenotypic distributions caused by plasticity. In the case where populations are unable to exhibit one of the aforementioned responses, extinction is the inevitable outcome. Scientists have recognized this issue and have worked tirelessly over the last 30 years to determine which species are vulnerable, how populations are responding to rapid environmental changes, and how to best conserve the most at-risk lineages. However, the efforts to predict how populations and species will persist after a century of consistent and strong climate change tend to ignore how these changes affect contemporary populations, and thus we risk missing the critical phenotypic trajectories that lead to rapid adaptation, range shifts, or extinction, which could provide both a platform for informing species conservation, but also enhance our knowledge of biodiversity. This dissertation explores how environmental variation over a variety of spatial and temporal scales impacts the selective environment in which species live, as well as the multiple plastic responses populations can exhibit in response to changing environmental conditions. First, the relationship between declining food availability and rising environmental 4 temperatures is quantified. Food availability exacerbates organismal performance and reduces the availability of populations to mount adaptive phenotypic changes in response to changing environments. Second, the relationship between thermoregulatory behavior and individual fitness is quantified. Fitness is increased when lizards exhibit warmer preferred temperatures and can sprint faster to enhance their thermoregulatory ability. Third, the efficacy of short-term plasticity in response to heat waves is quantified. Heat waves induce “hardening responses” which are stress-induced physiological mechanisms of surviving short-term and deleterious environmental fluctuations. Indeed, when these responses are elicited, other phenotypic traits suffer which trade-off with an individual’s ability to exploit the adaptive nature of plasticity. Last, population-level variation is quantified in climate-relevant traits for populations across an elevational gradient. Breaking from other studies, I find strong local adaptation consistent with the environmental differences across populations. Together, these findings provide new insights on the co-evolution of behavior and physiology, how traits respond to environmental variability, and the efficacy of different phenotypic response options that species can use to buffer the effects of climate warming. 5 DEDICATION For my dad. 6 ACKNOWLEDGMENTS This dissertation would not have been possible had my advisor, Don Miles, not taken a risk by accepting a student who had no experience researching the effects of climate change. His patience and willingness to work through my ideas will forever be appreciated. My dissertation committee, Shawn Kuchta, Willem Roosenburg, and James Dyer have provided strong and invaluable feedback, and for that I thank them. I would also like to acknowledge the past graduate students in the Department of Biological Sciences who have made this experience feel more like an adventure rather than school: Eric Gorscak, Ryan Felice, Vinny Farallo, Matt Lattanzio, Maggie Hantak, Paul Converse, Michelle Converse, Garrett Sisson, Tom Radomski, Melissa Liotta, Jann Nassif, Sam Gutherz, Rebecca Keogh, and Tyler Goerge. I thank my partner, Meredith Fitschen-Brown, for her unconditional support. Finally, financial support for my dissertation data collection was provided by the Ohio University Graduate Student Senate, Ohio University Student Enhancement Award, National Audubon Society, Society for Integrative and Comparative Biology, American Philosophical Society, Explorer’s Club, and the Ohio Center for Ecology and Evolutionary Studies. 7 TABLE OF CONTENTS Page Abstract ............................................................................................................................... 3 Dedication ........................................................................................................................... 5 Acknowledgments............................................................................................................... 6 List of Tables ...................................................................................................................... 8 List of Figures ..................................................................................................................... 9 Chapter 1: Food, Temperature, and Endurance: Effects of Food Deprivation on the Thermal Sensitivity of Physiological Performance .......................................................... 10 Introduction ................................................................................................................. 10 Methods....................................................................................................................... 15 Results ......................................................................................................................... 20 Discussion ................................................................................................................... 26 Chapter 2: Natural Selection on Thermal Preference, Critical Thermal Maxima, and Locomotor Performance ................................................................................................... 34 Introduction ................................................................................................................. 34 Methods....................................................................................................................... 39 Results ......................................................................................................................... 45 Discussion ................................................................................................................... 49 Chapter 3: Antagonistic Responses of Exposure to Sublethal Temperatures: Adaptive Phenotypic Plasticity Coincides with a Reduction in Organismal Performance .............. 54 Introduction ................................................................................................................. 54 Methods....................................................................................................................... 58 Results ......................................................................................................................... 65 Discussion ................................................................................................................... 71 Chapter 4: Spatiotemporal Variation in Thermal Niches Suggests Lability Rather Than Conservatism of Thermal Phyisology Along an Environmental Gradient ....................... 78 Introduction ................................................................................................................. 78 Methods....................................................................................................................... 82 Results ......................................................................................................................... 88 Discussion ................................................................................................................... 95 References ....................................................................................................................... 103 8 LIST OF TABLES Page Table 1. Morphological statistics for fasted and fed lizards............................................... 21 Table 2. Fasting effects on thermal tolerance traits............................................................ 21 Table 3. Model selection analysis of fasting effects on performance curves..................... 26 Table 4. Thermal traits of surviving and deceased lizards after selection.......................... 46 Table 5. Selection differentials (s), coefficients (B), and effect sizes................................ 47 Table 6. Stabilizing/disruptive and correlational selection coefficients............................. 49 Table 7. Summary stats for body size and body temperatures across populations............. 89 Table 8. Operative temperature variation along an elevational gradient............................ 90 Table 9. Thermal performance
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