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Factors Affecting Metabolism During Non-Feeding Stages in Insects

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Factors Affecting Metabolism During Non-Feeding Stages in Insects FACTORS AFFECTING METABOLISM DURING NON-FEEDING STAGES IN INSECTS A Dissertation Submitted to the Graduate Faculty of the North Dakota State University of Agriculture and Applied Science By Liz Doralyn Cambron In Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY Major Program: Cellular and Molecular Biology April 2020 Fargo, North Dakota North Dakota State University Graduate School Title FACTORS AFFECTING METABOLISM DURING NON-FEEDING STAGES IN INSECTS By Liz Doralyn Cambron The Supervisory Committee certifies that this disquisition complies with North Dakota State University’s regulations and meets the accepted standards for the degree of DOCTOR OF PHILOSOPHY SUPERVISORY COMMITTEE: Dr. Kendra Greenlee Chair Dr. Stephen Foster Dr. Tim Greives Dr. Yagna Jarajapu Dr. George Yocum Approved: July 9, 2020 Dr. Kendra Greenlee Date Department Chair ABSTRACT Although feeding is important for optimal development and growth in insects, there are several points during the insect life cycle that are non-feeding: metamorphosis, pupation, and overwintering. Non-feeding periods also occur in response to internal cues, such as feedback from nutrient thresholds and immune responses being activated. Additionally, as an insect goes through different developmental stages, its nutritional requirements change in response to or in preparation for non-feeding periods. Most physiological responses like feeding are regulated through an interconnection of pathways, but how these networks change in response to different energy demands, such as immune challenges or changes in metabolism, is poorly understood. One significant pathway that is involved in regulating several physiological processes is the insulin signaling pathway. In my dissertation research, I tested hypotheses explaining the regulation of physiological processes during non-feeding periods in two agriculturally relevant insects, Manduca sexta and Megachile rotundata. First, I investigated how internal cues such as dietary lipid content and immune challenges cause non-feeding periods in M. sexta. Then, I investigated how insulin signaling regulates development during a non-feeding period like overwintering changes in M. rotundata. Since the insulin signaling (IIS) pathway is critical for development and growth, I focused on testing if this pathway plays a role in regulating non- feeding periods. My research showed that increased dietary lipid content causes a cessation of feeding, which suggests there is a possible lipid threshold that when reached, causes M. sexta to switch from lipid consumption for storage to lipid excretion. When looking at another cue like immune challenges, my results showed that during a bacterial infection, a Toll-mediated suppression of IIS pathway may be regulating feeding and causing a non-feeding period exhibited as sickness-induced anorexia. Lastly, my results also showed that the IIS pathway is iii suppressed in overwintering M. rotundata, and that this process can change in response to temperature. Overall, my dissertation research showed that the insulin signaling pathway and nutrient content play a vital role in regulating non-feeding periods. Investigating insulin signaling, lipid metabolism, and innate immunity in these species closes a gap in knowledge of invertebrate development. iv ACKNOWLEDGEMENTS I would like to first and foremost acknowledge my family, God, and my partner Dr. Jamie Kopco, for being my rock through this all and never giving up on me. My advisor Dr. Kendra Greenlee for seeing the potential in me, supporting my crazy research ideas, and being the best academic mom any student could ask for. Her continuous support and encouragement definitely made a difference in my graduate career. My PhD committee members, Dr. Tim Greives, Dr. Stephen Foster, and Dr. Yagna Jarajapu for their continuous support and guidance. I also would like to acknowledge the Greenlee lab members that have been with me on this journey. Dr. Kimi Booth, Dr. Megan Bennett, Dr. Mia Park, Dr. Giancarlo Lopez-Martinez, Taylor Lundquist, Kayla Earls, Georgia Starr Davis, Korie DeBardlabon, and the several undergraduate students that have helped me over the years. Each and every single one of them have helped me grow both professionally and personally over the past six years. My USDA mentors, Dr. Joseph Rinehart and Dr. George Yocum, for pushing me to reach for the stars, guiding me through my graduate career and helping me plan for life after my PhD, and adopting me as their lab daughter. Dr. Dacotah Melicher was also a vital support with his knowledge on bioinformatics and continuous encouragement. The Insect Cryobiology and Ecophysiology (ICE) group for their feedback, knowledge, support, and positive community. I would also like to acknowledge my biological sciences family, the faculty, Wendy Leach, Chad Lachowitzer, and Jeff Kittilson, for all of their help, guidance, support, and patience. I definitely have to acknowledge my writing group gang who spent hours in person and over zoom calls to write with me, allowing me to vent, and providing feedback and support for the past 4 years: Dr. Jessica Graham, Dr. Aubrey Sirman, Dr. Rebecca Young, Dr. Tara Slominski, Michelle Angelucci, Monica Anderson-Berdal, and Nik Snyder. I also need to acknowledge a few other v graduate students at NDSU that truly helped me through my PhD like Dr. Matthew Crouse, Dr. Faithe Keomanivong, Dr. Jiyan Mohammed, Courtney Grula, and Heather North. Lastly, I would like to acknowledge a handful of other support systems that have played a key role in my success: NDSU graduate school, NDSU counseling center and graduate support group, my health coach team, my sorority sisters of Gamma Phi Omega Int’l Inc., and other family and friends. During my PhD I was fortunate enough to be funded by fellowships and grants, including from North Dakota State University, EPSCoR grant to KJG, and the National Science Foundation. vi DEDICATION This PhD is dedicated to my family for all their sacrifices, patience, support, and help in getting my through these past six years. My motivation for this PhD always was my nieces and nephews, so this is to show them that 1) we can do whatever we sent our minds to, 2) we are not a product of our circumstances, and 3) hard work will always trump talent. I would also like to dedicate this to all the first generation Americans and students. Several of us started our journeys by putting ourselves out there and looking for opportunities on our own. We continuously fight for our dreams without a road map, so we create our own. This is also dedicated to all the other students who battle with their mental health every day. Your worth is not determined by your productivity. Your mental illness does not make you any less smart. Have patience with the journey and with yourself. And remember, there is always something to live for. Always. vii TABLE OF CONTENTS ABSTRACT ................................................................................................................................... iii ACKNOWLEDGEMENTS ............................................................................................................ v DEDICATION .............................................................................................................................. vii LIST OF TABLES ........................................................................................................................ xii LIST OF FIGURES ..................................................................................................................... xiii LIST OF APPENDIX TABLES ................................................................................................. xvii LIST OF APPENDIX FIGURES............................................................................................... xviii CHAPTER 1. REGULATION OF PHYSIOLOGICAL PROCESSES BY THE INSULIN SIGNALING PATHWAY IN INSECTS ....................................................................................... 1 Overview ..................................................................................................................................... 1 Insect development ...................................................................................................................... 2 Holometabolous life cycle ....................................................................................................... 2 Diapause and overwintering .................................................................................................... 2 Insect nutrition ............................................................................................................................. 4 Nutrient requirements for development................................................................................... 4 Carbohydrates .......................................................................................................................... 5 Lipids ....................................................................................................................................... 6 Amino acids ............................................................................................................................. 6 Nutrient regulation................................................................................................................... 7 Role of the fat body ................................................................................................................
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