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The Role of Maternal Hormones in Programming Offspring

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The Role of Maternal Hormones in Programming Offspring THE ROLE OF MATERNAL HORMONES IN PROGRAMMING OFFSPRING AGGRESSION by ALEXANDRA B. BENTZ (Under the Direction of Kristen J. Navara) ABSTRACT Over the past few decades, researchers have come to recognize that a mother’s physiological response to her environment can have transgenerational effects. Females transfer testosterone to their young prenatally and this maternal effect makes offspring more aggressive. Aggression can strongly influence an animal’s success depending on environmental context, and maternal effects are an important source of variation in aggressive behavior; yet, we do not fully understand what shapes maternal hormone responses or the proximate mechanisms that mediate its effects. While it is generally assumed that females in competitive environments allocate more testosterone, adaptively creating more aggressive offspring, not all bird species (in which maternal effects are best studied) respond by allocating more testosterone to egg yolks, making it hard to predict how different bird species’ behaviors and egg components will respond to environmental change. Additionally, we do not know what mechanisms mediate the effects of prenatal testosterone on offspring behavior, preventing us from understanding how it fits into larger ecological and evolutionary frameworks. Hence, my dissertation addressed 1) the causes of interspecies variation in yolk testosterone allocation in competitive environments and 2) the molecular mechanisms facilitating behavioral plasticity in offspring exposed to prenatal testosterone. For Aim 1, I performed a meta-analysis to identify species-specific traits influencing yolk testosterone allocation (Chapter 2) and experimentally tested the findings (Chapter 3). I found that colonial species do not allocate more yolk testosterone in competitive environments, unlike solitary species. This work challenges a widely held assumption that this maternal effect is characterized by a uniform response to competition, showing that it should be contextualized with life-history traits. Next, I explored natural variation in molecular responses to yolk testosterone in a wild songbird (Chapter 4) and experimentally tested the mechanisms in a captive species (Chapter 5). Hundreds of neural genes are differentially expressed in offspring exposed to yolk testosterone, including genes in behavioral pathways (e.g., nitric oxide and serotonin). Additionally, the data suggest epigenetic mechanisms may play a role in mediating the effects of maternal testosterone on offspring phenotype. Ultimately, this work helps us better understand the environmental and molecular causes of phenotypic plasticity. INDEX WORDS: yolk testosterone, aggressive behavior, avian, maternal effect, competitive environment, DNA methylation THE ROLE OF MATERNAL HORMONES IN PROGRAMMING OFFSPRING AGGRESSION by ALEXANDRA B. BENTZ BS, Appalachian State University, 2010 MS, Appalachian State University, 2012 A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY ATHENS, GEORGIA 2017 © 2017 Alexandra B. Bentz All Rights Reserved THE ROLE OF MATERNAL HORMONES IN PROGRAMMING OFFSPRING AGGRESSION by ALEXANDRA B. BENTZ Major Professor: Kristen Navara Committee: Woo Kim Andrew Benson Sonia Altizer Lynn Siefferman Electronic Version Approved: Suzanne Barbour Dean of the Graduate School The University of Georgia August 2017 ACKNOWLEDGEMENTS I want to thank Dr. Kristen Navara for her support and expertise as I completed this dissertation and for pushing me to achieve my full potential. I would also like to acknowledge Dr. Lynn Siefferman who has continued to play a pivotal role in my development as a scientist, Dr. Wendy Hood for her understanding early in my academic career, and Drs. Andy Davis, Woo Kim, and Andrew Benson for the guidance you provided me as committee members. I also could not have completed this research without the help and feedback from Dr. Elizabeth Pusch, Dr. Nicola Khan, Jay Curry, Elizabeth Wrobel, Caroline Cummings, and Tori Andreasen. Additionally, I have had the pleasure of collaborating with many fantastic scientists to complete this dissertation, so thank you Aubrey Sirman, Dr. Haruka Wada, Dr. Chad Niederhuth, and Dr. Laura Carruth. I would also like to thank Ryan Hudgins, Luke Bridges, Andrew Arnold, Fernando Mateos-Gonzalez, and the Navara and Hood laboratory undergraduate students who helped to complete the aviary and field work components of this research. Furthermore, this research would not have been possible without funding from the National Science Foundation (NSF) Graduate Research Fellowship and Doctoral Dissertation Improvement Grant (#1601396), and research grants from the Animal Behavior Society, Society for Integrative and Comparative Biology, American Ornithologists’ Union, North American Bluebird Society, and Kaytee Pet Products. Finally, I would like to thank my family and friends, especially Katie Rifenburg and Erin Abernathy, all of whom never cease to be there for me emotionally and also to remind me how to have a good time, and my partner, Daniel Becker, whose invaluable collaborative input and unconditional support have made me a better scientist and a happier person. iv TABLE OF CONTENTS Page ACKNOWLEDGEMENTS ........................................................................................................... iv LIST OF TABLES ........................................................................................................................ vii LIST OF FIGURES ..................................................................................................................... viii CHAPTER 1 INTRODUCTION AND LITERATURE REVIEW .....................................................1 2 EVOLUTIONARY IMPLICATIONS OF INTERSPECIFIC VARIATION IN A MATERNAL EFFECT: A META-ANALYSIS OF YOLK TESTOSTERONE RESPONSE TO COMPETITION .................................................................................8 3 THE EFFECTS OF CONSPECIFIC AGGRESSION ON MATERNAL TESTOSTERONE ALLOCATION IN A COLONIAL SPECIES .............................31 4 RELATIONSHIP BETWEEN MATERNAL ENVIRONMENT AND DNA METHYLATION PATTERNS OF ESTROGEN RECEPTOR ALPHA IN WILD EASTERN BLUEBIRD (SIALIA SIALIS) NESTLINGS: A PILOT STUDY ............45 5 MOLECULAR MECHANISMS MEDIATING THE EFFECTS OF PRENATAL TESTOSTERONE ON ADULT AGGRESSIVE PHENOTYPES .............................68 6 CONCLUSIONS..........................................................................................................92 REFERENCES ..............................................................................................................................96 APPENDICES A CHAPTER 2: SUPPLEMENTAL INFORMATION ................................................136 v B CHAPTER 4: SUPPLEMENTAL INFORMATION ................................................145 C CHAPTER 5: SUPPLEMENTAL INFORMATION ................................................150 vi LIST OF TABLES Page Table 2.1: Univariate rankings of mixed-effects models (MEMs) predicting effect size for the relationship between competitive environment and yolk testosterone response for the (a) full and (b) reduced dataset ................................................................................................27 Table S2.1. Details of species included in the meta-analysis, including the Fisher’s Z transformed effect size and both study- and species-specific moderators ...........................................137 Table 4.1: Linear regression analyses of the percent DNA methyaltion of each CpG site in the putative promoter region of estrogen receptor alpha in 14 day old Eastern Bluebird offspring in the diencephalon and telencephalon with yolk testosteorne concentration as the predictor variable. ........................................................................................................64 Table S4.1. All potential transcription factor binding sites (matrix similarity >72%) on the putative Eastern Bluebird (Sialia sialis) ERα promoter region according to MatInspector (Genomatix). ....................................................................................................................146 Table S5.1. Most overrepresented biological processes from the list of genes differentially expressed between offspring from testosterone-injected eggs. ........................................154 Table S5.2. Behavioral genes associated with aggression that are significantly differentially expressed between individuals from control and testosterone-injected eggs ..................159 Table S5.3. Linear regression models for the relationship between average aggression score and scaled log(1+FPKM) data (Z-score).. ..............................................................................160 vii LIST OF FIGURES Page Figure 2.1: Phylogenetic visualization of mean yolk testosterone response per species included in the main analyses ...............................................................................................................28 Figure 2.2: Distribution of effect sizes for relationships between competitive environment and yolk testosterone response (Fisher’s Z ± 95% confidence intervals). ................................29 Figure 2.3: Distribution of effect sizes according to (a) coloniality and (b) nest type. .................30 Figure S2.1. Flow diagram for documenting the data collection and inclusion process according to PRISMA style ..............................................................................................................138
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