Sociogenomics of maternal care and parent-offspring coadaptation in the European earwigs (Forficula auricularia) Inauguraldissertation zur Erlangung der Würde eines Doktors der Philosophie vorgelegt der Philosophisch-Naturwissenschaftlichen Fakultät der Universität Basel von Min Wu aus China Zürich, 2018 Originaldokument gespeichert auf dem Dokumentenserver der Universität Basel edoc.unibas.ch Genehmigt von der Philosophisch-Naturwissenschaftlichen Fakultät auf Antrag von Fakultätsverantwortlicher: Prof. Dr. Dieter Ebert, Professor, Universität Basel Dissertationsleiter: Dr. Mathias Kölliker, Universität Basel Dr. Jean-Claude Walser, ETH, Zürich Korreferent: Prof. Dr. Michel Chapuisat, Universität Lausanne Basel, den 15.11.2016 Prof. Dr. Jörg Schibler, Dekan 2 ACKNOWLEDGEMENTS I would like to thank all the people involved in my PhD work in one way or another. First, great thanks to Mathias Kölliker and Jean-Claude Walser for the opportunity studying such a super exciting project as well their patient supervision and strengthful support to conquer all the challenges throughout my PhD. Special thank to Dieter Ebert for taking me into the daphnia group during the last year of my PhD, and all the support and advice he gave to finish my original project and for future plans on academic career. Thanks to Michel Chapuisat for being the external referee of my defense all the way from Lausanne. And thanks for his detailed comments and corrections of my thesis. I thank Anne Roulin for all the collaboration in the first chapter, sharing first co-authorship in the publication and her advice regarding bioinformatic analysis in the second chapter. Thanks to Roberto Arbore for showing me how to extract RNA firsthand, Simone Kühn-Bühlmann for showing me how to dissect the tiny delicate earwig brain. All molecular work and bioinformatic analysis were done at Genetic Diversity Centre (GDC) ETH, Zürich. I thank Aria Minder, Silvia Kobel, Katja Eschbach, Niklaus Zemp and Stefan Zoller for their suggestions and support in GDC. I also thank Christian Beisel for his contribution on RNA-Seq sequencing at the Quantitative Genomics Facility (QGF) in ETH, Basel. I thank Lina Sandrin for taking me to GDC for the first time for molecular work at ETH, Zürich, Stefan Boos for help with GC-MS and support in the earwig lab together with Lilian Röllin. I thank all the people mentioned above in the earwig group and Philip Suess, Xiuyun Tang, Shirley Raveh, and Dominik Vogt and Janine Wong for their help, support, discussions and fun in the lab and office. Thanks to former group member Joël Meunier for his comments on the manuscript of Chapter2. Thanks Louis Du Pasquier, Gilberto Bento Neves, Jing He and Christina Grozinger for their advice 3 concerning RNA interference, Jürgen Hotitnger for laboratory support. Thanks to Lei Sun as the co- author of my second chapter for the successfully cloning of earwig genes for ds-RNA synthesis within extremely limited time frame restricted by eariwg reproductive season (only twice a year), and collecting phenotypic data in the earwig lab. Thanks to Sebastian Bonhoeffer and Martin Ackermann for providing their microbial lab at ETH, Zürich for gene cloning. It would be impossible for me to accomplish the RNAi experiment without any of them. I thank everyone in the daphnia group for accepting me being part of it. Thank Yasmin Picton, Urs Stiefel and Lukas Zimmermann for their support regarding administrative, laboratory and computer related issues respectively. I also thank Walter Salzburger for his help and support including during the block course Evolutionary Biology when I was supervising student project in the first year of my PhD. I would thank everyone at the Zoological Institute for all the discussions and inspirations. Thanks to all the people who has been part of the ProDoc program. It was a great collaboration and regular meetings between groups studying cooperation all over Switzerland. From that I learned a lot about theories and empirical studies in terms of understanding the proximate and ultimate cause of cooperation, met excellent researchers in this field from within Switzerland as well as abroad, and contributed to the organization of several events for the students being on board of the student committee during the first year of my PhD. Thanks to the Swiss National Science Foundation for funding my PhD project. Thanks to the EMBL CPP fellowship and travel grant from University of Basel for financial aid when attending conferences and presenting my PhD work. Thanks to Laurent Keller for encouraging the application of my PhD extension when the original contract was about to terminate and the successful extension enabled the further functional study of candidate genes identified in RNA-Seq experiment. Last but not least, I would thank my family for their support, especially my husband not only for a life companion but also for academic discussions and being in the lab with me during weekends and midnights when I was busy with my experiments. 4 Table of Contents SUMMARY...............................................................................................................................................7 GENERAL INTRODUCTION.............................................................................................................10 CHAPTER 1...........................................................................................................................................17 De novo Transcriptome Hybrid Assembly and Validation in the European Earwig......................................17 Non-earwig and transposable element sequences.......................................................................21 Completeness of the hybrid assembly.........................................................................................22 Identification and annotation of the earwig protein core set......................................................24 Validation of the transcriptome and candidate gene expression analysis...................................27 CHAPTER 2...........................................................................................................................................44 The Genetic Mechanism of Selfishness and Altruism in Parent-Offspring Coadaptation............................44 Comparative transcriptomics......................................................................................................46 Two genes underlying parent-offspring coadaptation.................................................................48 Characterize the social function of Th and PebIII with RNAi.....................................................48 Regulations between insulin signaling- juvenile hormone-vitellogenin......................................50 CHAPTER 3...........................................................................................................................................68 Transgenerational Effects of Maternal Care on Parental-Offspring Coadaptation......................................68 Transgenerational effect on the expression of Th and PebIII......................................................74 Transgenerational effect on fitness.............................................................................................75 CHAPTER 4...........................................................................................................................................84 Preprogrammed Expression of Parent-Offspring Coadapted Genes in Earwig Mothers.............................84 Validation of RNA-Seq with Fluidigm gene expression dynamic array.......................................87 Preprogrammed expression of Th and PebIII.............................................................................89 CONCLUDING REMARKS................................................................................................................96 APPENDIX I........................................................................................................................................101 Parent–Offspring Conflict and the Genetic Trade-offs Shaping Parental Investment................................101 Direct response to selection in mothers....................................................................................105 Correlated response to selection in offspring...........................................................................105 Shape of the genetic trade-offs..................................................................................................107 5 APPENDIX II.......................................................................................................................................119 Genetics and Developmental Biology of Cooperation....................................................................................119 Models of inheritance of cooperation.......................................................................................121 Genetic and molecular pathways underlying cooperation........................................................130 Neurobiological mechanisms of cooperation............................................................................132 Developmental regulation of sociality/cooperative behaviour..................................................133 6 SUMMARY Conflict and cooperation are ubiquitous in nature and in animal families where parents and offspring reciprocally influence each other's behavior and fitness. Evolutionary models predict selection for parent-offspring