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Download in Flybase to Acquire Gene Ontology Terms UC Irvine UC Irvine Electronic Theses and Dissertations Title Diversification and expression of vision-related genes in Lepidoptera Permalink https://escholarship.org/uc/item/0br612qw Author Macias Munoz, Aide Publication Date 2018 License https://creativecommons.org/licenses/by-nd/4.0/ 4.0 Peer reviewed|Thesis/dissertation eScholarship.org Powered by the California Digital Library University of California UNIVERSITY OF CALIFORNIA, IRVINE Diversification and expression of vision-related genes in Lepidoptera DISSERTATION submitted in partial satisfaction of the requirements for the degree of DOCTOR OF PHILOSOPHY in Ecology and Evolutionary Biology by Aide Macias Muñoz Dissertation Committee: Professor Adriana D. Briscoe, Chair Associate Professor Kevin Thornton Associate Professor Ali Mortazavi 2018 Chapter 1 © 2016 Molecular Biology and Evolution Chapter 2 © 2017 Genome Biology and Evolution All other materials © Aide Macias Muñoz DEDICATION To my parents, Maria and Raymundo, whose sacrifices and hard work have made this possible. Your courage has inspired me to be brave in pursuing my career goals. Your strength has motivated me to work hard and your kindness has taught me to be caring. Your love and support have been monumental in my educational pursuit. DEDICATORIA Para mis padres, María y Raymundo, cuyos sacrificios y trabajo duro han hecho esto posible. Su valor me ha inspirado a ser valiente en perseguir mis objetivos profesionales. Su fuerza me motiva a trabajar duro y su amabilidad me ha enseñado bondadosa. Sobre todo, su amor y apoyo han sido monumental en mi búsqueda educativa. ii TABLE OF CONTENTS Page LIST OF FIGURES iv LIST OF TABLES v ACKNOWLEDGMENTS vi CURRICULUM VITAE viii ABSTRACT OF THE DISSERTATION x INTRODUCTION 1 CHAPTER 1: Transcriptome-wide differential gene expression in Bicyclus anynana butterflies: Female vision-related genes are more plastic 14 CHAPTER 2: Copy number variation and expression analysis reveals a non-orthologous pinta gene family member involved in butterfly vision 74 CHAPTER 3: Phototransduction in Lepidoptera 138 CONCLUSIONS 208 iii LIST OF FIGURES Page Figure 1.1 Photographs of adult Bicyclus anynana heads and heatmaps of diffentially expressed (DE) contigs by seasonal form and sex. 45 Figure 1.2 Functional enrichment of differentially expressed genes. 46 Figure 1.3 Expression of differentially expressed genes across seasonal forms. 47 Figure 1.4 Opsin expression in B. anynana seasonal forms. 49 Figure 1.5 Reverse-transcription PCR (RT-PCR) of eye and brain tissue. 50 Figure 1.6 Eye development gene networks. 51 Figure 2.1 Bayesian phylogeny of insect CRAL-TRIO domain proteins. 106 Figure 2.2 CRAL-TRIO domain gene location and patterns of mRNA presence or absence. 107 Figure 2.3 Expression of CRAL-TRIO domain genes. 109 Figure 2.4 Hme CTD31 RT-PCR. 110 Figure 2.5 Hme CTD31 Western Blot. 111 Figure 2.6 Immunohistochemistry of Hme CTD31 in H. melpomene eye and optic lobe. 112 Figure 3.1 Proposed model of the lepidopteran phototransduction cascade. 167 Figure 3.2 Differential expression analysis. 168 Figure 3.3 Opsin gene family. 169 Figure 3.4 DAGL gene family. 170 Figure 3.5 TRP gene family. 171 Figure 3.6 Wunen gene family. 172 Figure 3.7 Vha-100 gene family 173 iv LIST OF TABLES Page Table 1.1 Summary of findings from Everett et al. (2012). 52 Table 1.2 Summary of the total number of differentially expressed (DE) contigs and unique gene ontology (GO) terms discovered in analyses. 53 Table 1.3 BLAST results for contigs with opsin-like expression patterns. 54 Table 1.4 Significant P values of two-factor ANOVAs for eye development, phototransduction, and eye pigment genes. 55 Table 2.1 Summary of differentially expressed (DE) and upregulated contigs. 113 Table 2.2 Expression patterns of CRAL-TRIO domain contigs. 114 Table 2.3 Top 20 proteins from upper, middle and lower bands detected by mass spectrometry sorted by upper band Mascot score. 115 Table 3.1 Summary of transcriptome-wide analysis. 174 v ACKNOWLEDGMENTS First and foremost, I would like to thank my wonderful advisor Dr. Adriana Briscoe for her support and guidance throughout my PhD. Her mentorship has been vital to my academic success and I will forever cherish the advice she has given me and all that she has taught me. She embodies what it means to be a great researcher, teacher, and mentor. I am grateful to my committee members Dr. Kevin Thornton, Dr. Ali Mortazavi, and Dr. Francisco Ayala. Their profound knowledge of the fields of evolution, development, and genetics was invaluable in helping me determine rigorous tests for my hypotheses. Their advice during committee meetings helped me improve figures and motivated me to aim high when submitting journals. I am also grateful for the advice and mentorship provided Dr. JJ Emerson who advised me on project development and analysis. I would also like to thank my collaborator and co-author Dr. Antónia Monteiro for her intellectual contributions and advice in completing chapter 1 of my dissertation. I would like to thank faculty, postdocs, students and staff in the Ecology and Evolutionary Department who have made working at UC Irvine a fun and stimulating experience. Their love of science and friendly demeanors have been inspiring. Dr. Kate Loudon and Dr. Donovan German always provide motivating conversation at department events and Mahul Chakraborty, Joe Heras, and Jim Baldwin-Brown are always willing to discuss molecular and bioinformatic techniques. I am thankful for Spanish nights with current and past students Alejandra Rodriguez, Will Petry, Adriana Romero, Kyle McCulloch, Alberto Soto, Wilnelia Recart, and Ana Catalán. I am also thankful for family dinners with Jimmy Kezos, Caitlin Looby, Thomas Barter, Grant Rutledge, and Mark Phillips. I was extremely lucky to have Mark Phillips as a colleague, neighbor, and friend. Thank you for bringing me lemons when I was sick, for picking me up after midnight once when I had to stay in lab late, and for all of the cheer up dinners. I am thankful to have had some awesome and brilliant lab members throughout the years. Kyle McCulloch, Susan Finkbeiner, Gilbert Smith, Ana Catalán, Jennifer Briner, Aline Rangel, and Zachary Johnson have given essential feedback on my presentations and writing. Gil was a colleague and a mentor; our discussions of data analysis and project design have helped shape me into the scientist that I have become. I have had the privilege to work closely with Gil, Ana and Aline to co-author publications and I admire their work ethic and value their help and input. Thank you Kyle for making every day in lab enjoyable. Your constructive criticism and encouragement made me a better and more confident scientist. I am honored to have worked alongside you for five years. I look forward to future collaborations. I was lucky to have you as a labmate and friend. I will always treasure the memories of our salsa dancing experiences, gossip sessions, and our conference stories. vi This dissertation would not be possible without the love and support of my friends and family. I was lucky to attend graduate school near my large Macias family and had the chance to see them often. Thank you all for your joy. Interacting with you reminds me of the importance of hard work. While I do not see the Muñoz family as often, I can feel your love and support, thank you for believing in me. My sister Rubi Macias is my hero and I can only hope one day to be as fierce as she is. I cannot thank my parents Raymundo and Maria Macias enough for everything that they do for my sister and me. Rubi and I owe our accomplishments to your sacrifices and lessons. I would also like to thank my bestie Richard Garcia who makes light of everything and makes me happy every time we talk or spend time together. I want to thank Imran Khan for motivating and pushing me these past few months. I am grateful to have an amazing group of powerful women in my life. Verenice Bravo’s carefree attitude encourages me to be brave and take risks. Nicole Campos is someone who I can always talk to about professional and personal problems; her wise advice has been priceless. Brittaney de la Torre has been both a source of emotional support and entertainment, thank you for tolerating my multiple musings via text every single day. Diana Gutierrez has been like a sister, thank you for providing a listening ear when I need it and for being an amazing best friend. The four of you motivate me to be successful and kind, our conversations ground me and remind me that it’s important to give back to our community. Finally, I would like to thank the funding sources that made this dissertation research possible. Fellowship support was provided by the National Science Foundation Graduate Research Fellowship Program and by the Ford Predoctoral Fellowship Program. Additional fellowship support was provided by the William D. Redfield Graduate Fellowship Award. I am grateful for travel support from the Broadening Participation Committee Travel Award, Charlotte Mangum Student Support, UC Irvine Associated Graduate Student Travel Grant, BEACON Center Travel Award and support from the Society for the Study of Evolution. vii CURRICULUM VITAE Aide Macias Muñoz EDUCATION 2018 University of California Irvine, CA Ph.D. in Ecology and Evolutionary Biology 2015 University of California Irvine, CA M.S. in Ecology and Evolutionary Biology 2011 University of California Berkeley, CA B.A. in Integrative Biology PUBLICATIONS Smith G, Kelly JE, Macias-Muñoz A , Butts CT, Martin RW, Briscoe AD. 2018. Evolutionary and structural analyses uncover the role of novel gene duplications in pollen feeding butterflies.
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