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REGENERATION in the PILIDIUM by NICOLE DEETTE MOSS a THESIS

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REGENERATION in the PILIDIUM by NICOLE DEETTE MOSS a THESIS REGENERATION IN THE PILIDIUM by NICOLE DEETTE MOSS A THESIS Presented to the Department of Biology and the Graduate School of the University of Oregon in partial fulfillment of the requirements for the degree of Master of Science September 2017 THESIS APPROVAL PAGE Student: Nicole DeEtte Moss Title: Regeneration in the Pilidium This thesis has been accepted and approved in partial fulfillment of the requirements for the Master of Science degree in the Department of Biology by: Svetlana Maslakova Advisor George von Dassow Member Richard Emlet Member and Sara D. Hodges Interim Vice Provost and Dean of the Graduate School Original approval signatures are on file with the University of Oregon Graduate School. Degree awarded September 2017 ii © 2017 Nicole DeEtte Moss iii THESIS ABSTRACT Nicole DeEtte Moss Master of Science Department of Biology September 2017 Title: Regeneration in the Pilidium Ability to regenerate is found in many groups of metazoans but the majority of research is focused on adults from just a few taxa, such as planarians and hydra (Agata and Inoue, 2012; Bely et al., 2014). Increasing the diversity of study organisms and life stages can reveal new and interesting aspects of regeneration mechanisms. This study focuses on regeneration of the nemertean pilidium larva. The planktotrophic pilidium of Maculaura alaskensis provides a unique model in which to observe several components of the regeneration process. Here I have documented a timeline for regeneration and have begun to evaluate the cells responsible for regenerative success. This study has revealed the interplay between regeneration and degeneration, a tradeoff between larval and juvenile structures, as well as the important relationship between global versus local signaling in proliferation and differentiation responses. iv CURRICULUM VITAE NAME OF AUTHOR: Nicole DeEtte Moss GRADUATE AND UNDERGRADUATE SCHOOLS ATTENDED: University of Oregon, Eugene DEGREES AWARDED: Master of Science, Biology, 2017, University of Oregon Bachelor of Science, Biology, 2012, University of Oregon AREAS OF SPECIAL INTEREST: Regeneration Developmental Biology Evolution of Development Molecular and Cell Biology PROFESSIONAL EXPERIENCE: Graduate Research Assistant, Oregon Institute of Marine Biology, University of Oregon, 2015-2017 Graduate Teaching Fellow, Oregon Institute of Marine Biology, University of Oregon, 2016 GRANTS, AWARDS, AND HONORS: 1st Place Poster, Graduate Research Forum, 2017 Best Student Paper, American Microscopical Society, 2017 v ACKNOWLEDGMENTS I have been lucky to have several great mentors through my academic career – Teresa Villa ignited my interest in biology and Eric Selker introduced me to the excitement of research. My greatest support has been from my advisor, Svetlana Maslakova. She is the scientist I aspire to be. She introduced me to the diversity of developmental strategies and the elegance of the pilidium larva. She has enhanced my experience by including me on projects outside this work and has taken me on the most incredible adventures. Thank you for indulging in my interest in regeneration and inspiring a life long appreciation for biological diversity. Thank you to my committee members George von Dassow and Richard Emlet. George showed me the art in microscopy and reminded me to always look closely and pay attention. My work greatly benefitted from Richard’s perspective and push to evaluate problems from a different mindset. I have felt incredibly welcomed and supported by the OIMB community during my time as a graduate student and an undergraduate in 2011. Thank you to all the faculty and our enthusiastic librarian, Barb Butler, who is always available to discuss books, biology, and bicycles. Special thank you to Maya Wolff-Watts for introducing me to marine biology and the Oregon Institute of Marine Biology during an introductory course in 2010. I would also like to thank the OIMB graduate student community including Mackenna Hainey, Zofia Knorek, Caitlin Plowman, Alexa Romersa, Mike Thomas, Jenna Valley, Reyn Yoshioka and in particular Carly Salant and Ella Lamont who I started this journey with just over two years ago. You have proven to be dedicated colleagues and incredible friends. A special thank you to Kara Robbins for always being prepared for ‘outside science’ and an early morning in the mudflats. Finally, thank you to my family and friends. I am lucky to have such an incredible support system. To Lindsey Holman for always knowing exactly what to say, even from 3,000 miles away. To my adventure buddy, Melinda Wheelock, for countless hours spent discussing biology over cups of coffee (or flights of beer), reading just about every draft I’ve written, and for exploring every coast with me. To Alyssa Moss, the first person I want to call whenever I have exciting news. Thank you to my Aunt Robin, my first best friend and second mom. Thank you to my parents, Paul and Nancy Moss, you have whole vi heartedly supported my every adventure and crazy idea. Thank you for encouraging me to work hard and for always cheering for the Ducks. You inspire me and fuel my love of exploration. vii TABLE OF CONTENTS Chapter Page I. INTRODUCTION .................................................................................................... 1 II. REGENERATION IN THE PILIDIUM ................................................................. 3 Introduction ............................................................................................................ 3 Nemerteans and the Pilidium Larva ................................................................. 3 Observation of Regeneration in the Pilidium ................................................... 4 Regeneration of Two Distinct Structures ......................................................... 5 Methods.................................................................................................................. 6 Collecting Adults and Culturing Larvae .......................................................... 6 Microsurgery.. .................................................................................................. 7 Serotonergic Neurons and Muscle Labeling .................................................... 7 BrdU Assay and Visualization ......................................................................... 8 Serotonergic Neurons and EdU Chase ............................................................. 10 Microscopy ...................................................................................................... 10 Measurements .................................................................................................. 11 Image Analysis ................................................................................................. 11 Statistics ........................................................................................................... 12 Results .................................................................................................................... 12 Regeneration Success ....................................................................................... 12 Lateral Lappet Regeneration ............................................................................ 13 Source Cells for Lappet Regeneration ............................................................. 18 viii Chapter Page Apical Organ Regeneration .............................................................................. 20 Source Cells for Apical Organ Regeneration ................................................... 23 Discussion .............................................................................................................. 23 Lateral Lappet Regeneration ............................................................................ 24 Variation in Apical Organ Regeneration ......................................................... 27 Comparison of Regeneration in Two Different Larval Structures ................... 29 Developmental Plasticity of the Pilidium ........................................................ 30 III. CONCLUSION ...................................................................................................... 31 REFERENCES CITED ................................................................................................ 33 ix LIST OF FIGURES Figure Page 1. Lappet regeneration in a wild caught pilidia ......................................................... 4 2. BrdU pulse-chase workflow. ................................................................................. 9 3. Lappet and apical organ regeneration success ....................................................... 12 4. Lappet regeneration after complete (A-F) and partial (G-L) lappet removal .................................................................................................................. 14 5. Structural recovery of lappet (A-E) including collar cells (D’), muscle (E’), marginal ciliary nerve (A’’-E’’) and the origin of serotonergic neurons in the regenerated lappet .................................................................................................. 15 6. Measurements of lappet regeneration including ciliary band length (A), lappet surface area (B) and extrapolated cephalic imaginal disc volume (C) ...... 17 7. Proliferation in response to lappet removal, (A) comparison of proliferation on the left and right sides of an individual larva, (B, F) immediately following lappet microsurgery, (C,G) 24h, (D, H) 48h, (E, I) 4-days
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