Evolution of Central Complex Development: Cellular and Genetic Mechanisms

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Evolution of Central Complex Development: Cellular and Genetic Mechanisms Evolution of central complex development: cellular and genetic mechanisms Dissertation for the award of the degree “Doctor rerum naturalium” of the Georg-August-Universität Göttingen within the doctoral program Genes and Development of the Georg-August University School of Science (GAUSS) submitted by Max Stephen Farnworth from Hanau, Germany Göttingen, 2019 Thesis Advisory Committee Prof. Dr. Gregor Bucher (advisor) (University of Göttingen; Department of Evolutionary Developmental Genetics) Prof. Dr. Halyna Shcherbata (Hannover Medical School; Institute for Cell Biochemistry) Prof. Dr. André Fiala (University of Göttingen; Department of Molecular Neurobiology of Behavior) Members of the Examination Board First reviewer: Prof. Dr. Gregor Bucher (University of Göttingen; Department of Evolutionary Developmental Genetics) Second reviewer: Prof. Dr. Halyna Shcherbata (Hannover Medical School; Institute for Cell Biochemistry) Further Members of the Examination Board Prof. Dr. André Fiala (University of Göttingen; Department of Molecular Neurobiology of Behavior) Prof. Dr. Christoph Bleidorn (University of Göttingen, Department of Animal Evolution and Biodiversity) PD Dr. Roland Dosch (University Medical Center Göttingen, Department of Developmental Biochemistry) Prof. Dr. Ralf Heinrich (University of Göttingen, Department of Cellular Neurobiology) Date of Oral Examination: September 30th, 2019 i DECLARATION I hereby declare that the doctoral thesis entitled "Evolution of central complex development: cellular and genetic mechanisms" has been written independently and with no other sources and aids than quoted. ______________________ Göttingen, July 11th, 2019 ii For my family iii Acknowledgements First of all, I want to thank Prof. Gregor Bucher for the opportunity of a doctoral thesis as well as his optimism and patience. During a period of life with a lot of changes, you have helped and supported me with a good mixture of kindness and firm guidance. I greatly acknowledge scientific help and support by my thesis committee members, Profs. Halyna Shcherbata and André Fiala. I thank Elisa Buchberger for suffering through her role as my coffee partner and for her kind honesty and calming presence. I am so glad we became friends, as GIF-infused as possible. I want to thank Dr. Nico Posnien for being a role model in how to balance all the different aspects of the scientific with the private life. But even more, we have ideas together, that we bravely (or naively?) put into practice. I want to thank Kolja N. Eckermann for teaching me all the basics of Molecular Biology I should have known before I entered the lab and, together with Dr. Peter Kitzmann, for showing me the way of delicious coffee making. I thank Dr. Peter Kitzmann for being such a good lab colleague with mad sport skills, integrity and the ability, together with Kolja, to come up with nicknames that stick, annoyingly, even four years after their invention. I want to acknowledge all the help I received from Elke Küster, Claudia Hinners and Dipl.- Ing. Beate Preitz. Particularly Elke has set up so many single crosses of flies and beetles for me, with incredible patience for my lack of planning – thank you! I want to thank Dr. Marita Buescher for helpful scientific input and for entertaining me through odd and surprisingly funny stories of her life, including a lot of cat stories... I acknowledge the tremendous help by Dr. Felix S.C. Quade for all things 3D reconstruction. I want to thank Luisa Mathilde Welp, Marvin Seifert, Lara Markus and Ehecatl A. Ruiz Alvarez for their experimental help. I acknowledge tremendous last-minute help by Ann-Kathrin Müller in correcting this work. Of course, all lab members of both departments deserve a big thank you. From all of you I have profited, in some shape or form! Particularly though Birgit Rossi, Merle Eggers, Bettina Hucke, Angelika Löffers, Helma Gries, Dhaval Patel, Prof. Ernst A. Wimmer, Prof. Sigrid Hoyer- Fender, Dr. Gerd Vorbrüggen, Dr. Ufuk Günesdogan, Hassan M. M. Ahmed, Dr. Bernhard G. M. Schmid (so many nice chats!), Dr. Stefan Dippel, Julia Kurlovich, Mila Ilic, Dr. Micael Reis, Martin Milner (see you next Tuesday!), Dr. Vera Terblanche, Magdalena Schacht (all the food!), Felix Kaufholz, Dr. Salim Ansari, Dr. Salim M. Hakeemi, Dominik Mühlen, Dr. Daniela Grossmann, Dr. Jürgen Dönitz and Dr. Bicheng He. iv Financial support from the Göttingen Graduate Center for Neurosciences, Biophysics, and Molecular Biosciences (GGNB) is greatly appreciated. I want to take the opportunity to acknowledge people not involved in this work: First of all, thanks for the advice, help and guidance, particularly by Prof. Martin Plath – who let me discover this ‘brain evolution’ topic of mine, Prof. Robert A. Barton – from whom I learned how to critically read and discuss topics, but also Dr. Roland Dosch, Dr. Stephen H. Montgomery and Prof. Julia Fischer for guidance on critical thinking, topical support and reflection. I further want to acknowledge financial support during my Master’s Studies by the German National Academic Foundation. Through Prof. Sarah Köster’s mentorship, inspired courses by Profs. Peter Kappeler and Daniel Haun, and support by Prof. Katja Liebal, I was able to stay motivated pursuing an academic career. I want to thank my friend Martin Meschkat. We cannot stop testing each other’s statements, positions, and reflecting on each other’s emotional stupidity and personal fallacies. I learn a lot from and with you. Oh, and you and my Billyard pal Dr. David Brockelt proof-read this thesis – thank you, and, I am so sorry! So many more friends would be needed to be listed here with special mention, but the two pages are nearly full, so in short: Christian, Katha, Seb, Hannes, Daniel, Lena, Mo, Luisa and Johanna – thank you so much! Last and most importantly, my family: My father, Peter, is the reason why I studied biology, why I have a ‘scientist’s’ mind (or at least pretend to have) and I am incredibly thankful for your support throughout. My mother, Wilma, is my role model for all the life skills I continue to fail at. I couldn’t be prouder to be your son. My brother, Christopher: it is a luxury to have someone who you know will always have your back, no matter what. I am thankful to my brother Mark, for trying to teach me to believe in myself and to be more relaxed. I do not know what he would say to me having completed a doctoral thesis, but I hope he would have been proud. My daughter Lilith has changed my life for the better. Her existence has not only changed my daily life, but how I think and how I exist. I am a much better person because of her. My girlfriend, friend, life-partner and wife Tina: I still cannot believe that we not only share a life and family together, but that you believe in me. Without your support, I wouldn’t have been able to do this work. v TABLE OF CONTENT 1. SUMMARY ..................................................................................................................... - 1 - 2. INTRODUCTION .......................................................................................................... - 2 - 2.1. The diversity of brain evolution ........................................................................................... - 2 - 2.2. Insect brains are suitable subjects for evolutionary research ............................................... - 4 - 2.3. Comparing development of brains between insect species ................................................. - 6 - 2.4. The use of genetic neural lineages and alternative marking strategies ............................... - 7 - 2.5. Using CRIPSR/Cas to generate transgenic lines in alternative model organisms ............ - 10 - 2.6. A beetle – fly comparison ................................................................................................... - 10 - 2.7. My doctoral work contained in three manuscripts and their contributions....................... - 11 - 3. RESULTS ...................................................................................................................... - 13 - 3.1. MANUSCRIPT 1: SEQUENCE HETEROCHRONY BETWEEN DROSOPHILA AND TRIBOLIUM CAUSES EMERGENCE OF A PRECOCIOUS LARVAL FORM OF THE CENTRAL COMPLEX - 14 - 3.1.1. ABSTRACT ......................................................................................................................... - 16 - 3.1.2. INTRODUCTION .................................................................................................................. - 17 - 3.1.2.1. Insect brain evolution – Diversity in a conserved architecture .......................................... - 17 - 3.1.2.2. Heterochrony is a mechanism in the evolution of development with a largely unknown cellular basis ...................................................................................................................... - 18 - 3.1.2.3. Structure and function of the central complex ................................................................... - 18 - 3.1.2.4. The central complex is developed by conserved cellular mechanisms .............................. - 20 - 3.1.2.5. Central complex heterochrony – deviation from a common program? ............................. - 21 - 3.1.2.6. A comparison of the development of insect brains using genetic neural lineages ............ - 22 - 3.1.2.7. Using Tribolium and Drosophila as model systems for a comparison based on a common toolkit ................................................................................................................................
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