University of Tennessee, Knoxville TRACE: Tennessee Research and Creative Exchange Doctoral Dissertations Graduate School 12-2018 Life history and contemporary evolution: Implications for managing a hybrid salamander invasion Evin Timothy Carter University of Tennessee, [email protected] Follow this and additional works at: https://trace.tennessee.edu/utk_graddiss Recommended Citation Carter, Evin Timothy, "Life history and contemporary evolution: Implications for managing a hybrid salamander invasion. " PhD diss., University of Tennessee, 2018. https://trace.tennessee.edu/utk_graddiss/5237 This Dissertation is brought to you for free and open access by the Graduate School at TRACE: Tennessee Research and Creative Exchange. It has been accepted for inclusion in Doctoral Dissertations by an authorized administrator of TRACE: Tennessee Research and Creative Exchange. For more information, please contact [email protected]. To the Graduate Council: I am submitting herewith a dissertation written by Evin Timothy Carter entitled "Life history and contemporary evolution: Implications for managing a hybrid salamander invasion." I have examined the final electronic copy of this dissertation for form and content and recommend that it be accepted in partial fulfillment of the equirr ements for the degree of Doctor of Philosophy, with a major in Ecology and Evolutionary Biology. Benjamin M. Fitzpatrick, Major Professor We have read this dissertation and recommend its acceptance: Arthur Echternacht, Benjamin Keck, Daniel Simberloff Accepted for the Council: Dixie L. Thompson Vice Provost and Dean of the Graduate School (Original signatures are on file with official studentecor r ds.) Life history and contemporary evolution: Implications for managing a hybrid salamander invasion A Dissertation Presented for the Doctor of Philosophy Degree The University of Tennessee, Knoxville Evin Timothy Carter December 2018 Copyright © 2018 by Evin Timothy Carter All rights reserved. ii DEDICATION To Zoe iii ACKNOWLEDGEMENTS First and foremost, I thank Lindsey Hayter for her love and support, for her long afterwork hours helping to care for hundreds of salamanders in the lab that each of us would much rather have finding (and not collecting) in the field, and just sticking with me through this degree. I thank my family for their continued support and generating my interest in nature and conservation in the first place, and I extend special thanks to Bryan Eads and Ryan Hunt for their friendship and help with fieldwork. I am forever grateful to Dana Bland for her immense generosity in not only helping me obtain access to several field sites, but also joining me in the field, allowing me to use her equipment, and loaning out her personal truck for trips across California on multiple occasions for weeks at a time. Sincerely, I cannot thank you enough. I extend particular thanks to my adviser, Ben Fitzpatrick, for providing much of the groundwork that made this work possible and, as usual, pretending that his graduate students were not his most substantial annoyance. I also thank Dan Simberloff, Robert Washington-Allen, and Brad Shaffer for their invaluable advice and guidance throughout my dissertation. Sandy Echternacht, Joe Bailey, Jim Fordyce, Ben Keck, and Annette Summers-Engel also provided valuable advice and edits on proposals and dissertation drafts at various stages. Joel Corush and Matthew Niemiller offered helpful discussion that has steered many aspects of my dissertation and related work. NSF funding that permitted the most enjoyable aspects of my dissertation likely would not have been possible without assistance from many you above. Countless undergraduates and interns helped make the work here possible. I extend the most gratitude to Jacob Wessels, Jonathan Cox, Justin Baldwin, John Hill, Shawn McClurg, and Tristan Gregory for endless an painstaking care of laboratory colonies of tiger salamanders. I also offer special thanks to Michael Hobbs for his assistance with fieldwork that helped make Chapter II and Chapter III possible as well as Matthew Chaney for his dedication to habitat surveys and construction and placement of dozens of temperature loggers into 1-meter-deep ‘soil’ during peak drought conditions in Central iv California [read: he spent hours digging tons of holes in ‘concrete’ by hand], which provided the environmental data that set Chapter II in motion. Alan Launer facilitated and provided several hours of assistance during vernal pond surveys on multiple occasions at Stanford University’s Lake Lagunita and adjacent vernal pond complex, and Kate Guerena with USFWS assisted with and facilitated tiger salamander breeding pond surveys at San Luis and Merced National Wildlife Refuge. I thank Gage Dayton and Sean McStay (and the University of California Natural Reserve System) for providing camping accommodations, storage space, and even office space free of charge while conducting field work in California. Bruce Delgado and Eric Morgan (Bureau and Land Management) as well as Bart Kowalski worked diligently to facilitate salamander breeding pond surveys, habitat mapping, and deployment of temperature loggers across Fort Ord National Monument. Michael Sears provided laboratory space and respirometry equipment for the work presented in Chapter II, and Eric Riddell provided the most involved contribution to Chapter II as he was both active in and committed to the design and operation of respirometry trials. I thank Ronnie and Janeane Boggner for their hospitality and facilitiating multiple years of surveys on the former 5-Star Fish Farm in Clearlake Oaks, CA, where I was able to collect the only pure introduced Barred Tiger Salamanders. Many others in the Department of Ecology and Evolutionary Biology and the Biological Services Facility worked hard to make various aspects of my time a UTK go smoothly, particularly EEB administrative staff and several folks in BSF who handled orders and environmental chamber repairs Funding for this work was provided in by a number of public and private sources, but these include most notably, the National Science Foundation and the University of Tennessee Knoxville. v ABSTRACT Predicting adaptive responses of populations is a primary goal of evolutionary ecology and conservation. While evolution on contemporary time scales is now apparent, the underlying mechanisms and whether change is adaptive or neutral often remain unclear. Typically, habitat modification, introduction of nonnative taxa, hybridization, or a combination of these factors is invoked to explain rapid evolution. I focus on an amphibian system of conservation concern to explore the interplay between ecology and evolution in shaping population genetic structure, including how habitat and physiology interact with life history to promote invasion success. I begin by using simulation to demonstrate that the mode and tempo of evolution is highly subject to interactions between genome structure and life history strategy. I show that incorporating high reproductive outputs characteristic of amphibians can increase the probability that selection and recombination result in highly fit multilocus genotypes, but complex life cycles characteristic of pond-breeding taxa can simultaneously increase the probability that low-fitness combinations drift rapidly to fixation, highlighting the possibility that rapid "adaptation" in small populations might sometimes be explained by drift. I then explore environment-dependent selection in a hybrid zone involving obligately-metamorphic California Tiger Salamanders (Ambystoma californiense) and nonnative Barred Tiger Salamanders (A. mavortium) having a more plastic facultatively- paedomorphic life history. I consider measures of physiological performance that are expected to affect amphibian population dynamics, evaluating whether metabolic and water loss rates are consistent with hybrid advantage or disadvantage (and transgressive segregation) under conditions experienced during key life history events. Alternating patterns of hybrid advantage linked to high energy demand and plastic life history result in bounded hybrid superiority and, as yet, a clear limit to the geographic spread of hybrid genotypes. Next, I show that recent abrupt declines in hybrid population success are likely associated with high energy demand alongside drought- induced reductions in resources, where many [facultatively paedomorphic] hybrid populations experienced pond-drying for the first time since their initial invasion. In contrast, obligately-metamorphic natives that evolved in a drought-prone landscape did vi not experience apparent declines. These results underscore integrating scientific disciplines as requisite to effective conservation science and invasion management. vii TABLE OF CONTENTS INTRODUCTION ............................................................................................................. 1 Hybrid Invasions .......................................................................................................... 1 The challenges ......................................................................................................... 1 Focal System: Introgressive hybridization between an imperiled native salamander and its introduced congener ........................................................................................ 2 Life history strategy and adaptive evolution ................................................................. 3 Complex life history .................................................................................................