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Epigenetic Mechanisms Governing Behavioral Reprogramming in the Ant Camponotus Floridanus

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Epigenetic Mechanisms Governing Behavioral Reprogramming in the Ant Camponotus Floridanus University of Pennsylvania ScholarlyCommons Publicly Accessible Penn Dissertations 2018 Epigenetic Mechanisms Governing Behavioral Reprogramming In The Ant Camponotus Floridanus Riley John Graham University of Pennsylvania, [email protected] Follow this and additional works at: https://repository.upenn.edu/edissertations Part of the Genetics Commons, Molecular Biology Commons, and the Neuroscience and Neurobiology Commons Recommended Citation Graham, Riley John, "Epigenetic Mechanisms Governing Behavioral Reprogramming In The Ant Camponotus Floridanus" (2018). Publicly Accessible Penn Dissertations. 2883. https://repository.upenn.edu/edissertations/2883 This paper is posted at ScholarlyCommons. https://repository.upenn.edu/edissertations/2883 For more information, please contact [email protected]. Epigenetic Mechanisms Governing Behavioral Reprogramming In The Ant Camponotus Floridanus Abstract Eusocial insect colonies divide behaviors among specialist groups called castes. In some species, caste identity is determined by the interaction of endogenous (e.g. genomic) and exogenous (e.g. juvenile hormone from nurses) signals during larval development, suggesting epigenetic mechanisms underlie plastic traits tied to caste identity. Previous work demonstrated a link between patterns of histone H3 lysine 27 acetylation (H3K27ac) and caste-specific gene expression in Major and Minor workers of the ant Camponotus floridanus, and we hypothesized caste-specific behaviors such as foraging may be similarly regulated by histone acetylation. To test this hypothesis, we fed mature (~30d old) Majors and Minors with histone deacetylase inhibitors (HDACi), and CBP-dependent histone acetyl transferase inhibitors (HATi). We observed foraging enhancement after HDACi, and foraging suppression after HATi in Minors. Curiously, we did not observe increased foraging in HDACi treated mature (~30d) Majors. However, HDACi injections in callow (0-1d old) Majors succeeded in causing stable reprogramming of foraging behavior, indicating a critical period, or ‘window’ of epigenetic sensitivity to HDACi exists in young majors. To address this possibility, we injected Majors with HDACi in a time course and observed juvenile (d0-d5) Majors are susceptible to reprogramming, whereas mature (d10) Majors are not. To assess innate differences in the brain between castes, we conducted an RNA-seq study in untreated Major and Minor workers 0, 5, and 10 days old, and detected caste-specific patterns of juvenile hormone and ecdysone signaling. Finally, to characterize the transcriptional and epigenetic effects of reprogramming, we conducted RNA-seq in HDACi treated Major brains, and detected consistent upregulation of members of the neuron restrictive silencing factor (NRSF/REST) repressive complex (e.g. CoREST, RPD3, ttk). Notably, the top downregulated gene after HDACi is juvenile hormone esterase (JHe), which antagonizes JH signaling and inhibits foraging behavior in many eusocial insects. Thus, our results suggest REST/ CoREST mediated repression of JHe may be a significant source of stable changes to foraging in behaviorally reprogrammed Majors. Degree Type Dissertation Degree Name Doctor of Philosophy (PhD) Graduate Group Biology First Advisor Shelley L. Berger Keywords Behavior, Epigenetic, Eusocial, Histone modification, Neuroepigenetic, Reprogramming Subject Categories Genetics | Molecular Biology | Neuroscience and Neurobiology This dissertation is available at ScholarlyCommons: https://repository.upenn.edu/edissertations/2883 EPIGENETIC MECHANISMS GOVERNING BEHAVIORAL REPROGRAMMING IN THE ANT CAMPONOTUS FLORIDANUS Riley John Graham A DISSERTATION in Biology Presented to the Faculties of the University of Pennsylvania in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy 2018 Supervisor of Dissertation ______________ Shelley L. Berger Daniel S. Och University Professor, Professor of Cell and Developmental Biology and Professor of Biology Graduate Group Chairperson _________________ Michael Lampson Associate Professor of Biology and Graduate Chair in Biology Dissertation Committee Nancy Bonini, Florence R.C. Murray Professor of Biology Roberto Bonasio, Assistant Professor of Cell and Developmental Biology Mia Levine, Assistant Professor of Biology Timothy Linksvayer, Associate Professor of Biology DEDICATION I dedicate this work to Elizabeth, for passing her love for science and nature on to her sons. And to Olivia, for breathing new life into us all. May this thesis help you along your own journey. And to Colleen, who treated the students in her care to unwavering kindness and support. ii ACKNOWLEDGMENT I am indebted to my advisor, Shelley L. Berger, who has been a courageous advocate for her students, our ant models, and the epigenetics community. I am entirely grateful for her support. I would like to thank Nancy Bonini, Roberto Bonasio, Mia Levina, and Tim Linksvayer for their insightful comments and suggestions that helped mold this work into its best form. Dr. Linksvayer welcomed me into the Penn community, and invited me out to find ants in Fairmount Park. I’m proud to have spent time with him in the field, in classrooms, and in his lab. I would like to thank Doris Wagner and Michael Lampson, who have been exceptionally supportive and accessible graduate chairs, and always encouraged me to keep pushing ahead. Karl Glastad for assuming the role of energy in its purest form and sharing it around, etc. Cristina Brady for sustaining the colony (I don’t mean ants), and being a true friend. Dan Simola for his guru-level mentoring, and brilliant character. Free will is alive and well. iii ABSTRACT EPIGENETIC MECHANISMS GOVERNING BEHAVIORAL REPROGRAMMING IN THE ANT CAMPONOTUS FLORIDANUS Riley J. Graham Shelley L. Berger EusoCial insect colonies divide behaviors among specialist groups called castes. In some species, Caste identity is determined by the interaCtion of endogenous (e.g. genomic) and exogenous (e.g. juvenile hormone from nurses) signals during larval development, suggesting epigenetic mechanisms underlie plastic traits tied to caste identity. Previous work demonstrated a link between patterns of histone H3 lysine 27 acetylation (H3K27ac) and caste-specifiC gene expression in Major and Minor workers of the ant Camponotus floridanus, and we hypothesized caste-specific behaviors such as foraging may be similarly regulated by histone acetylation. To test this hypothesis, we fed mature (~30d old) Majors and Minors with histone deacetylase inhibitors (HDACi), and CBP-dependent histone acetyl transferase inhibitors (HATi). We observed foraging enhancement after HDACi, and foraging suppression after HATi in Minors. Curiously, we did not observe increased foraging in HDACi treated mature (~30d) Majors. However, HDACi injections in callow (0-1d old) Majors succeeded in causing stable reprogramming of foraging behavior, indicating a critical period, or ‘window’ of epigenetic sensitivity to HDACi exists in young majors. To address this possibility, we injected Majors with HDACi in a time course and observed juvenile (d0-d5) Majors are susceptible to reprogramming, whereas mature (d10) Majors are not. To assess innate differences in the brain between castes, we conducted an RNA-seq study in untreated Major and Minor workers 0, 5, and 10 days old, and detected caste-specific patterns of juvenile hormone and ecdysone signaling. Finally, to characterize the transcriptional and epigenetic effects of reprogramming, we conducted RNA-seq in HDACi treated Major brains, and detected consistent upregulation of members of the neuron restrictive silencing factor (NRSF/REST) repressive complex (e.g. CoREST, RPD3, ttk). Notably, the top downregulated gene after HDACi is juvenile hormone esterase (JHe), which antagonizes JH signaling and inhibits foraging behavior in many eusocial insects. Thus, our results suggest REST/CoREST- mediated repression of JHe may be a significant sourCe of stable changes to foraging in behaviorally reprogrammed Majors. iv TABLE OF CONTENTS DEDICATION ........................................................................................................................ II ACKNOWLEDGMENT ...................................................................................................... III ABSTRACT ..........................................................................................................................IV CHAPTER 1: INTRODUCTION ........................................................................................ 1 From Waddington to behavioral epigenetics ......................................................................................... 1 Epigenetic processes link gene expression and chromatin structure ..................................................... 2 The histone language and behavior ........................................................................................................ 3 Eusocial insects are new model organisms for behavioral epigenetics .................................................. 4 Caste identity involves changes in gene expression and hPTMs ............................................................ 5 Chapter 1 Bibliography .......................................................................................................................... 7 CHAPTER 2: EPIGENETIC (RE)PROGRAMMING OF CASTE-SPECIFIC BEHAVIOR IN THE ANT CAMPONOTUS FLORIDANUS ...................................... 11 Background .........................................................................................................................................
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