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University of Nevada, Reno Understanding Patterns of Resistance to Spider Venom in Lizards: Ecology and Phylogeny Matter A thesis submitted in partial fulfilment of the requirements for the degree of Master of Science in Biology By Vicki L. Thill Dr. Chris Feldman/Thesis Advisor Dr. Mike Teglas/Thesis Co-advisor December 2019 © by Vicki L. Thill 2019 All Rights Reserved THE GRADUATE SCHOOL We recommend that the thesis prepared under our supervision by VICKI LEE THILL entitled Understanding Patterns of Resistance to Spider Venom in Lizards: Ecology and Phylogeny Matter be accepted in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE Christoffer R. Feldman, Ph.D., Advisor Michael B. Teglas, Ph.D., Co-advisor Jennifer L. Hoy, Ph.D., Graduate School Representative David W. Zeh, Ph.D., Dean, Graduate School December 2019 i ABSTRACT Lizards and spiders often engage in predator-prey interactions, and many spiders can be dangerous as both predator and prey. However, we know little about how lizards tackle dangerous spider prey. And yet, some species are known to consume especially potent spider prey, like the western black widow (Latrodectus hesperus). In particular, Elgaria multicarinata is known to preferentially consume venom-defended L. hesperus. I asked whether E. multicarinata possessed resistance to the venom of L. hesperus and evaluated resistance at two levels of biological organization: at the whole animal level, and at the muscle tissue level. I included one other sympatric species that will eat L. hesperus when offered (Sceloporus occidentalis), and one sympatric species that is known prey of L. hesperus (Uta stansburiana). To evaluate the whole animal resistance, I used sprint speed performance; to evaluate muscle tissue resistance, I used comparative histology. Lizards were tested against either a control (sterile saline), “low” (1 mouse LD50), or “high” (5 mouse LD50) dose of black widow spider venom (BWSV). I found that E. multicarinata showed no response to any venom treatment, while U. stansburiana had tissue level responses for both low and high venom treatments and a whole animal response only for high venom treatment; S. occidentalis was somewhere in the middle, with no whole animal response and slight (but significant) muscle tissue response. Given the variety of responses in these three lizards across response levels (whole animal, tissue) and treatments (low, high), and the lack of drastic ii susceptibility in U. stansburiana, I then asked whether resistance to BWSV could be rooted deep in the squamate lineage (i.e. an ancestral trait of all lizards). I investigated this by testing for whole animal and muscle tissue resistance to BWSV using sprint speed performance and comparative histology on species representing a broader phylogenetic, ecological, and geographical scope of Squamate taxa. I found that insectivorous species (Coleonyx variegatus and Takydromus sexlineatus) were resistant to both low and high venom treatments at the whole animal, but not at the tissue level. I included a single herbivorous species, Iguana iguana, which showed drastic decreases in sprint performance and severe tissue responses for both low and high venom treatments. The variation in responses seen at different levels (whole animal, tissue) and at different treatments (low, high) combined with ecological traits, provides evidence that both ecology and phylogeny contribute to whether BWSV resistance is present, and at what level – whole animal and/or muscle tissue. iii ACKNOWLEDGEMENTS This work would not have been possible without the dual guidance of my major advisors, Dr. Chris Feldman and Dr. Mike Teglas, who have both perfected the art of helpful criticism. Their support and responsiveness throughout this project was invaluable, and I will be forever grateful for their kindness and their positive and uplifting attitudes. Their enthusiasm for science was contagious and created a wonderful, encouraging space within which to question, to formulate ideas, to learn from mistakes, and to get things done. I also thank Dr. Jennifer Hoy for valuable contributions as a committee member, especially in regard to her advice about whole animal performance and histology data extractions. I sincerely thank Dr. Matt Forister for thoughtful discussion regarding analyses. I am thoroughly grateful to the late Dr. Nate Nieto for his early contributions, especially in regard to pilot trials that helped establish the viability of this project. I also thank Kris Wild for early project advice on racing lizards and video processing software and Jake Holland for track design and construction. I thank Dr. Bob Hansen for providing open use of his beautiful photographs of Elgaria multicarinata, Sceloporus occidentalis, Uta stansburiana, and Latrodectus. To all those who assisted with field collection in any way, thank you (in no particular order): Erica Ely, Dr. Bobby Espinoza, Kristin McCarty, Dr. Emily Taylor, Jason Wurtz, Dr. Dean Leavitt, Jonathan DeBoer, Ally Xiong, Joshua Hallas, Daniel Moore and finally, Jeff Wilcox at Sonoma Mountain Preserve for not only iv hosting during collection excursions but also being a science mentor and knowing exactly where to find Elgaria in the “off season”. For assistance with live animal trials, video processing, and data extraction, I’d like to thank McKenzie Wasley, the most capable and cheerful lab tech and human being I’ve ever encountered; Leah Herbert and Molly McVicar, both of whom tackled the most tedious tasks without complaint; and live animal caregivers and lab techs Amber Durfee, Taylor Disbrow, Lizzy Sisson, Luke Mauer, and Gabrielle Blaustein. I thank the Office of Animal Resources for accessibility and advice regarding best practices for live animal care, in particular John Gray and Rebecca Evans, and the Institutional Animal Care and Use Committee for approval of live animal protocols. I thank Robert del Carlo and Jessica Reimche for their intelligent discourse, helpful feedback, and for providing a positive environment within which to work. For reassurance, informal advice and, sometimes, commiseration, I thank my office colleagues, especially Dr. Anne Espeset. For assisting with almost every step of this project, from field collection to performance trials and manuscript review, I thank Haley Moniz, who is genuine, quick-witted, and impressively organized; she is a real human bean and my best friend. Support for this research was provided by the UNR Graduate Student Association Research Grant program, the Society for the Study of Amphibians and Reptiles (travel award), as well as funds to CRF, including generous donations by Ron Aryel. v TABLE OF CONTENTS Abstract ................................................................................................................ i Acknowledgements ........................................................................................... iii Table of Contents ................................................................................................ v List of Tables.................................................................................................................. vii List of Figures .................................................................................................. viii Thesis Overview ................................................................................................. 1 Literature Cited ............................................................................................................. 6 Chapter 1. Preying dangerously: Black widow spider venom resistance in sympatric lizards ............................................................................................ 9 Abstract .......................................................................................................................... 9 Introduction .................................................................................................................. 10 Methods ........................................................................................................................ 15 Animal collection and care .................................................................................... 15 Whole-animal performance ................................................................................... 15 Analyses ............................................................................................................... 17 Comparative histology ............................................................................................ 18 Results .......................................................................................................................... 19 Whole-animal performance ................................................................................... 19 Comparative histology ............................................................................................ 21 Discussion .................................................................................................................... 24 Literature Cited ........................................................................................................... 29 Tables ........................................................................................................................... 34 Figures .......................................................................................................................... 40 Chapter 2. Spider venom resistance in lizards lingers across branches .....
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