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The Evolution of Termite Immunity

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The Evolution of Termite Immunity The evolution of termite immunity Inaugural-Dissertation to obtain the academic degree Doctor rerum naturalium (Dr. rer. nat.) submitted to the Department of Biology, Chemistry and Pharmacy of Freie Universität Berlin by Shulin He 2018 The doctorate studies were conducted under supervision of Prof. Dr. Dino P. McMahon from September 2014 to September 2018 in the Institute of Biology. 1st Reviewer: Prof. Dr. Dino P. McMahon 2nd Reviewer: Prof. Dr. Jens Rolff_____ date of defense: ____25. 10. 2018______ Acknowledgments First and foremost, I would like to express my sincere gratitude to my advisor Prof. Dr. Dino P. McMahon. It has been an honor to be his first PhD student. I appreciate his contribution of time, ideas and funding to my project and any related research. It is his patience, motivation and encouragement that helped me to finish this work. His broad knowledge and his excellent guidance to science helped me succeed my PhD. I would like to express many thanks to the following persons: Thorben, Stefania, Alejandra, James for their professional and personal help and advice. I want to thank Thorben and James for their help to improve this thesis. With their company, the time I spent over the last four years has become invaluable memories. I would like to sincerely thank the Rolff group at Institute of Biology that have contributed immensely to my personal and professional time during my PhD. I am grateful to Prof. Dr. Jens Rolff for his introduce, guidance, instructive advice, valuable professional comments, all of which improved my work and expanded my knowledge in science. His help and advice have excelled me in many other aspects. I am thankful to Dr. Paul R. Johnston for his great help, patient instructions and numerous discussions on bioinformatic analysis and in other ways. It is his guidance that made it possible for me to learn bioinformatics and analyze sequence data in my project. His advice on many other aspects also improved me and gave me courage to keep on. I would like to thank Renate Radek who provided important higher termite species which made a great improvement for my work. I also appreciate other members from that group: Alex, Baydaa, Bin, Christin, Guozhi, Miko, Regina, Sabine for their professional and personal advice and help during my PhD. I also would like to thank the following persons: Sophie, Luis, Bea from the Armitage group for their useful advice and company. My appreciation also goes to the colleagues of Bundesanstalt für Materialforschung und - prüfung where I did almost all my work over the last four years. I would like to thank Dr. Rüdiger Plarre for allowing me to use termites and for his help on improving my thesis. I want to thank Yvonne for providing much help on catching the termites for studies. I also would like to thank Annett, Ronald and Thomas Dimke for their help on performing experiments, collecting termites and other personal matters. I want to thank Kerstin for her help on the improvement of this thesis and many other personal matters. I would like to thank all other colleagues whose names are not listed here but gave me personal or professional help. It is a great honor to meet and work with them. The valuable time and experience with them will always be remembered. I would like to thank Prof. Dr. Zongqing Wang and Prof. Dr. Yanli Che from Southwest University, China, who provided much help on sampling subsocial cockroaches. They were very kind host, had valuable expertise on subsocial cockroaches, and provided students with space for performing experiment. It is a great pleasure to me to know them and collaborate with them. I also would like to thank Susan Mbedi and other members from Berlin Center for Genomics in Biodiversity Research for their professional help and host for all transcriptome sequencing. In addition, I want to acknowledge Benno and Christoph for their help and expertise in proteomics. I also want to thank Jan Šobotník for providing important samples of higher termites. I am grateful to many Chinese friends. My time in last four years was made enjoyable in large part also due to the time we spent together. It is a great pleasure to meet and have fun with them. Their company and support were valuable experiences that will be deeply remembered. I would like to thank my family for their enormous encouragement and support. Most of all, I want to thank my girlfriend, who stands by my side with her patience, encouragement and support. It was them who gave me courage to have this valuable experience and to finish this work. I want to acknowledge the Chinese Scholarship Council that provided me a four year PhD scholarship. At last, I also would like to thank a lot of people whose names are not listed here for any kind of help they provided during my PhD. Words are not enough to express my gratitude. Thank you all. Table of contents List of abbreviations ...................................................................................................................... General introduction .................................................................................................................... 1 1.1 Biology of termites .................................................................................................. 2 1.1.1 Phylogeny of termites ...................................................................................... 2 1.1.2 Termites as social insects ................................................................................ 3 1.2 Immunity in social insects ....................................................................................... 5 1.2.1 Individual immunity .......................................................................................... 6 1.2.2 Social immunity ................................................................................................ 7 1.2.3 Immunity in cockroaches.................................................................................. 8 1.2.4 Evolution of immunity in social insects ............................................................. 8 1.3 Aim of the thesis ..................................................................................................... 8 1.4 Description of project .............................................................................................. 9 Chapter I An expanded repertoire of immune genes in the cockroach Blatta orientalis as revealed by de novo transcriptome analysis ......................................................... 11 2.1 Abstract ................................................................................................................ 12 2.2 Introduction ........................................................................................................... 13 2.3 Material and Methods ........................................................................................... 15 2.4 Results .................................................................................................................. 19 2.4.1 Transcriptome statistics ................................................................................. 19 2.4.2 Immune related gene identification ................................................................ 20 2.4.3 Gene ontology enrichment analysis following immune challenge ................... 20 2.4.4 Immune gene regulation after infection .......................................................... 21 2.5 Discussion ............................................................................................................ 22 2.6 Acknowledgements ............................................................................................... 26 Chapter II Evolution of termite immunity during the transition of eusociality ............... 27 3.1 Abstract ................................................................................................................ 28 3.2 Introduction ........................................................................................................... 29 3.3 Materials and Methods .......................................................................................... 31 3.4 Results .................................................................................................................. 37 3.4.1 Transcriptome and annotation statistics ......................................................... 37 3.4.2 Phylogenetic analysis .................................................................................... 37 3.4.3 Expansion and contraction of immune gene families ...................................... 40 3.4.4 Immune response in termite castes and cockroaches .................................... 41 3.5 Discussion ............................................................................................................ 44 3.6 Acknowledgements ............................................................................................... 48 Charpter III Termite soldiers contribute to social immunity by synthesizing potent oral secretions .......................................................................................................................... 49 4.1 Abstract ................................................................................................................ 50 4.2 Introduction ........................................................................................................... 51 4.3 Materials and Methods .......................................................................................... 52 4.4
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