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The Evolution and Maintenance of the Color Polymorphism in Plethodon Cinereus

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The Evolution and Maintenance of the Color Polymorphism in Plethodon cinereus (Caudata: Plethodontidae) 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 Maggie M. Hantak August 2019 © 2019 Maggie M. Hantak. All Rights Reserved. 2 This dissertation titled The Evolution and Maintenance of the Color Polymorphism in Plethodon cinereus (Caudata: Plethodontidae) by MAGGIE M. HANTAK has been approved for the Department of Biological Sciences and the College of Arts and Sciences by Shawn R. Kuchta Associate Professor of Biological Sciences Florenz Plassmann Dean, College of Arts and Sciences 3 ABSTRACT HANTAK, MAGGIE M., Ph.D., August 2019, Biological Sciences The Evolution and Maintenance of the Color Polymorphism in Plethodon cinereus (Caudata: Plethodontidae) Director of Dissertation: Shawn R. Kuchta Color polymorphism is the presence of two or more distinct, genetically determined color morphs within a single interbreeding population. An underexplored question in color polymorphic species pertains to how distinct phenotypes are maintained within and among populations. Little work has been done to examine geographic patterns in polymorphisms, with most studies focusing on a single population. Mechanisms that may maintain polymorphisms include negative frequency dependent selection, spatiotemporal variation in selection, and gene flow among populations. Investigating these mechanisms in multiple populations provides insight into the processes underlying the maintenance of genetic variation within and among populations. The Eastern Red-backed Salamander, Plethodon cinereus, is widespread throughout northeastern North America, and has two common color morphs: striped and unstriped. Previous studies have suggested that the two color morphs of P. cinereus differ in many elements of their biology, including physiology, territoriality, and mating interactions. However, most studies focus on a single biological feature in a single population, so little is known about diversifying selection. In addition, the evolutionary processes that operate on the polymorphism in populations are not understood. 4 This dissertation examines multiple mechanisms that may be contributing to color morph maintenance in P. cinereus with replication over both space and time, including populations that vary from monomorphic to polymorphic. In chapter 1, I reviewed previous literature on co-adapted trait complexes in P. cinereus and provided an overview of the mechanisms that may be maintaining two color morphs. I suggested additional studies are necessary and I also conveyed the importance of studying the polymorphism in a geographic and phylogenetic context. In chapter 2, I investigated whether spatial and temporal variation in selection aids in color morph maintenance by examining whether the striped or unstriped morph was more camouflaged from the perspective of visual predators. I found that the unstriped morph was in general more conspicuous to potential predators, although the level of camouflage varied by population and season. In chapter 3, I aimed to identify the relationship between color morph frequency, genetic structure, landscape and environmental variables using a landscape genetic framework. The results suggested that a mix of gene flow, genetic drift, and selection interacted to maintain the striped/unstriped polymorphism. In chapter 4, I examined whether dietary partitioning characterized the two morphs over spatiotemporal scales. Across six populations and two seasons, there was spatial and temporal variation in diet. However, I found no evidence of diet differences between the morphs in polymorphic populations and no change in dietary breadth between polymorphic and monomorphic populations, demonstrating lack of dietary ecological release. Finally, in chapter 5, I investigated whether morphs assortatively mated by color and/or body size across geographically distinct populations that varied in color morph frequency. Across 5 the studied populations, I found evidence of random mating between color morphs, which may contribute to color morph maintenance within populations. In addition, I found geographic variation in size-assortative mating, which may have led to reproductive isolation among populations. Together, these studies provided information on how the morphs of P. cinereus are maintained and demonstrate the importance of studying color polymorphisms over spatial and temporal scales. 6 DEDICATION For my family and friends, whose love and support made this dissertation possible. 7 ACKNOWLEDGMENTS My advisor, Shawn Kuchta, was continuously kind and helpful during the duration of this work. I would not have made it to where I am today without his wonderful mentorship. I thank my committee: Willem Roosenburg, Harvey Ballard, Kelly Williams, and Joseph Johnson for valuable feedback on this dissertation. I would especially like to thank Kelly Williams for providing statistical guidance on multiple chapters of this dissertation. My collaborators, Carl Anthony and Cari Hickerson were essential in contributing to the development and implementation of this research. Kyle Brooks and Olivia Brooks were vital to completing many elements of this dissertation. They helped collect an extraordinary amount of ecological data in the field, as well as substantially contribute to further data collection in the laboratory. I would like to thank my family, especially my parents, Debbie and Jim Hantak and my partner, Dan Paluh, for believing in and supporting me. Melissa Liotta, Alayna Tokash, and Kaili Boarman provided emotional support. Much traveling was necessary for the completion of this dissertation, and I would like to thank Carl Anthony and Cari Hickerson for providing housing, as well as my parents, and Old Woman Creek National Estuarine Research Reserve (NERR). I worked in several incredible localities for the duration of my dissertation research: Chapin Forest Reservation, Case Western Reserve University Squire Valleevue Farm, Cuyahoga Valley National Park, Manatoc Scout Reservation, Edison Woods Metropark, Old Woman Creek NERR, East Harbor State Park, and the Heineman property on South Bass Island. I would like to thank everyone who permitted me to work at these properties. Financial support for this dissertation was provided by the 8 Ohio Center for Ecology and Evolutionary Studies (OCEES), the National Science Foundation, an Ohio University Student Enhancement Award, Ohio University Graduate Student Senate Grants, the Society for the Study of Evolution Rosemary Grant Award, the Ohio University Graduate Student Research Fund, Old Woman Creek travel grants, Ohio Biological Survey Small Grant awards, and the Society for the Study of Amphibians and Reptiles Grants in Herpetology Award. 9 TABLE OF CONTENTS Page Abstract ............................................................................................................................... 3 Dedication ........................................................................................................................... 6 Acknowledgments............................................................................................................... 7 List of Tables .................................................................................................................... 11 List of Figures ................................................................................................................... 12 Chapter 1: A Review of Color Polymorphism and Co-adaptations in the Eastern Red- backed Salamadner (Plethodon cinereus) ......................................................................... 13 Introduction ................................................................................................................. 13 Chapter 2: Predator Perception Across Space and Time: Relative Camouflage in a Color Polymorphic Salamander .................................................................................................. 25 Introduction ................................................................................................................. 25 Methods....................................................................................................................... 28 Results ......................................................................................................................... 32 Discussion ................................................................................................................... 37 Tables .......................................................................................................................... 42 Figures......................................................................................................................... 45 Chapter 3: Do Genetic Structure and Landscape Heterogeneity Impact Color Morph Frequency in a Polymorphic Salamander? ....................................................................... 48 Introduction ................................................................................................................. 48 Methods....................................................................................................................... 51 Results ......................................................................................................................... 56 Discussion ..................................................................................................................
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