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The Ecology and Endocrinology of Facultative Paedomorphosis

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The Ecology and Endocrinology of Facultative Paedomorphosis University of Mississippi eGrove Electronic Theses and Dissertations Graduate School 2019 Extended Adolescence: The Ecology and Endocrinology of Facultative Paedomorphosis Jason R. Bohenek University of Mississippi Follow this and additional works at: https://egrove.olemiss.edu/etd Part of the Biology Commons Recommended Citation Bohenek, Jason R., "Extended Adolescence: The Ecology and Endocrinology of Facultative Paedomorphosis" (2019). Electronic Theses and Dissertations. 1554. https://egrove.olemiss.edu/etd/1554 This Dissertation is brought to you for free and open access by the Graduate School at eGrove. It has been accepted for inclusion in Electronic Theses and Dissertations by an authorized administrator of eGrove. For more information, please contact [email protected]. EXTENDED ADOLESCENCE: THE ECOLOGY AND ENDOCRINOLOGY OF FACULTATIVE PAEDOMORPHOSIS A Dissertation presented in partial fulfillment of requirements for the degree of Doctor of Philosophy in the Department of Biology The University of Mississippi by JASON R. BOHENEK May 2019 i Copyright © 2019 by Jason R. Bohenek All rights reserved. i ABSTRACT Phenotypic plasticity is an adaptation to unpredictable environments whereby an organism of a single genotype may express more than one phenotype under differing environmental conditions. Phenotypic plasticity can manifest as polyphenisms, which is an extreme form of phenotypic plasticity that produces two or more discrete, alternative phenotypes. The expression of alternative phenotypes is controlled by biotic and abiotic environmental factors, which variably affect the strength and direction of phenotypic outcomes. Using a model polyphenic salamander, I sought to understand the ecological and hormonal processes that regulate alternative phenotype expression. The mole salamander (Ambystoma talpoideum) and eastern newt (Notophthalmus viridescens) are facultatively paedomorphic, which is a polyphenism with two alternative adult phenotypes: paedomorphs and metamorphs. Paedomorphs retain juvenile characteristics at sexual maturity (i.e., gills and an aquatic morphology), while metamorphs transition to terrestrial environments. The expressed phenotype depends on the environment context in which the larvae develop, with paedomorphosis often occurring under favorable aquatic conditions. I conducted a series of experiments to investigate the roles of population density, predator presence, hydroperiod, and stress hormones in regulating the expression of paedomorphosis. Results indicated the regulation of paedomorphosis through multiple ecological factors may be reducible to density-mediated effects, with a few notable exceptions. I also show that elevated stress hormones play a central role in regulating metamorphosis suggesting that all ecological factors affecting facultative paedomorphosis may funnel through a simple stress physiology framework. In conclusion, environmental factors ii affecting this polyphenism may share a common thread of inducing a stress response that initiates metamorphosis, thereby regulating phenotype in the population. iii LIST OF ABBREVIATIONS AND SYMBOLS °C Degrees Celsius α Significance level AICc Sample size corrected Akaike Information Criterion ANOVA Analysis of variance BOBL Best of a bad lot hypothesis cm Centimeter CORT Corticosterone, the primary amphibian stress hormone CRH Corticotropin-releasing hormone df Degrees of freedom DO Dissolved oxygen (mg/L) DP Dimorphic paedomorph hypothesis F Test statistic in ANOVA g Gram GLMM Generalized linear mixed model HPI Hypothalamic-pituitary-interrenal axis L Liter LMM Linear mixed model m Meter P Probability value used in null hypothesis testing PA Paedomorph advantage hypothesis iv PERMANOVA Permutational multivariate analysis of variance pH Measure of acidity; concentration of hydrogen ions SE Standard error t Test statistic for the t-test T3 Thyroxine T4 Triiodothyronine TDS Total dissolved solids TSH Thyroid stimulating hormone TRC Tyson Research Center UMFS University of Mississippi Field Station v ACKNOWLEDGEMENTS I would to thank Matthew Pintar, Lauren Eveland, Tyler Breech, and Reed Scott for assistance with field work. Also, I would like to thank Timothy Chavez, Rachel Kroeger, Brandon McDaniel, Zachary Mitchell, Randi Robison, and Nishant Rout for their assistance with field work throughout the years. William J. Resetarits Jr. provided guidance and feedback on experimental designs, analyses, and manuscripts, as did Jason Hoeksema, Christopher Leary, Howard Whiteman, and Gregg Davidson. This work would not be possible without support from the Tyson Research Center and Washington University in St. Louis, with special thanks to Kevin Smith and Barbara Schall, for allowing us to use their facilities. Also, Beth Biro helped substantially with collecting at the Tyson Research Center. I would also like to thank the University of Mississippi Graduate Student Council, University of Mississippi Field Station’s Luther Knight Graduate Student Research Fund, the University of Mississippi Department of Biology, and the Henry L. and Grace Doherty Foundation for financial assistance. Also, thank you to Scott Knight and the University of Mississippi Field Station staff for use of facilities and access to natural environments. Also, thank you to Rosemary Knapp for providing advice on running whole-body radioimmunoassay. Lastly, Lauren Fuller, B. Mikah, and B. Luxi provided emotional support. This research was approved by the University of Mississippi’s Institutional Animal Care and Use Committee (protocol 14-028) and the Mississippi Department of Wildlife, Fisheries, and Parks. vi TABLE OF CONTENTS Abstract ........................................................................................................................................... ii List of abbreviations and symbols ................................................................................................. iv Acknowledgements ........................................................................................................................ vi List of tables ................................................................................................................................... ix List of figures ...................................................................................................................................x Chapter 1: Introduction ..................................................................................................................1 Background ................................................................................................................................2 Study site ..................................................................................................................................16 Mesocosms ...............................................................................................................................17 Study system ............................................................................................................................18 Chapter 2: Initial density sets trajectory for density-dependent polyphenism thresholds ...........21 Abstract ....................................................................................................................................22 Introduction ..............................................................................................................................24 Methods....................................................................................................................................27 Results ......................................................................................................................................30 Discussion ................................................................................................................................34 Chapter 3: Are direct density cues, not resource competition, driving life history trajectories in a polyphenic salamander? ............................................................................................................38 Abstract ....................................................................................................................................39 Introduction ..............................................................................................................................41 Methods....................................................................................................................................46 Results ......................................................................................................................................52 Discussion ................................................................................................................................57 Chapter 4: Ambystoma have convergent plastic responses among alternative habitat types separate by small spatial scales .................................................................................................62 Abstract ....................................................................................................................................63 Introduction ..............................................................................................................................64 Methods....................................................................................................................................68 Results ......................................................................................................................................72
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