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This electronic thesis or dissertation has been downloaded from Explore Bristol Research, http://research-information.bristol.ac.uk Author: Moreno Medina, Sandra Carolina C Title: The molecular mechanisms of behavioural transitions in insect life-cycles General rights Access to the thesis is subject to the Creative Commons Attribution - NonCommercial-No Derivatives 4.0 International Public License. A copy of this may be found at https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode This license sets out your rights and the restrictions that apply to your access to the thesis so it is important you read this before proceeding. Take down policy Some pages of this thesis may have been removed for copyright restrictions prior to having it been deposited in Explore Bristol Research. However, if you have discovered material within the thesis that you consider to be unlawful e.g. breaches of copyright (either yours or that of a third party) or any other law, including but not limited to those relating to patent, trademark, confidentiality, data protection, obscenity, defamation, libel, then please contact [email protected] and include the following information in your message: •Your contact details •Bibliographic details for the item, including a URL •An outline nature of the complaint Your claim will be investigated and, where appropriate, the item in question will be removed from public view as soon as possible. THE MOLECULAR MECHANISMS OF BEHAVIOURAL TRANSITIONS IN INSECT LIFE-CYCLES Sandra C. Moreno-Medina A dissertation submitted to the University of Bristol in accordance with the requirements for the award of the degree of Doctor of Philosophy in the Faculty of Life Science (November 2019). Word Count: circa 65,000 ABSTRACT Phenotypic plasticity is one of the most important fundamental processes by which organisms adapt to changes in their environment. Alternative behavioural phenotypes emerge via the expression of shared genes from the same genome. These phenotypes are expressed at different stages of key life-history transitions, or when organisms perform distinct tasks as they shift flexibly from one behavioural state to another through their breeding cycle. The molecular mechanisms by which organisms shift between behavioural phenotypes are poorly understood. Here, I investigate the molecular mechanisms underpinning plasticity in three types of phenotypic transitions: a key life-history transition (transition from worker to queen, in the social wasp Polistes lanio), an evolutionary transition (how non-social ancestral behaviours may provide a mechanistic ground plan for the origins of division of labour and caste evolution in the social Hymenoptera, using the non-social wasp Ammophila pubescens), and a series of behavioural transitions through a nesting cycle (behavioural phases exhibited by A. pubescens during the nesting cycle). Finally, plastic phenotypes can arise when populations become isolated (e.g. due to habitat fragmentation) forcing them to exploit different resources; in my final chapter, I examine the genetic diversity and differentiation of A. pubescens across a fragmented landscape. My results show that key life-history transitions are characterised by distinct “transitional” molecular signatures, resembling those involved in cell reprogramming. Second, I found evidence that cycles of reproductive and provisioning behaviours may provide a mechanistic ground plan for the evolution of sociality. Third, I found that behavioural phases of the non-social wasp nesting cycles are defined by distinct molecular signatures during the provisioning phases, but otherwise very subtle molecular signatures for the other phases. Finally, I found little evidence of genetic differentiation in populations of A. pubescens, suggesting gene flow despite being in a fragmented habitat. In conclusion, phenotypic transitions are not only underpinned by simple shifts between molecular processes but also by elaborated changes in genomic signatures allowing organisms to adjust their behaviours responsively to their environments. ii iii Acknowledgements I thank the National Council on Science and Technology of Mexico (CONACYT) and Mexico’s minister of education (SEP) for funding my PhD studies. Thanks to the University of Bristol Alumni Foundation and the School of Biological Sciences for funding my research. Sincere gratitude to my supervisors, Dr Seirian Sumner for her advice, assistance, encouragement and patience in helping me complete this thesis. Without her help, I would not have been able to complete this work. Professor Jane Memmott (who adopted me in the middle of my PhD when my entire wasp colony (except me) migrated to UCL) for being inclusive and supervising me in my time alone in the Life Science Building. Fieldwork would not have been possible without the collaboration of National Trust which granted me permission to study and collect wasps in Hartland Moor, Studland and Godlingston Heath. Specifically, thanks to Michelle Brown who was my direct contact with National Trust. Thanks to The Genetics Society which funded my fieldwork in 2017, and to Lydia Rowland who assisted me in the same year. To the Sumner lab who kindly made me part of the group. Robin Southon, Adam Devenish, Patrick Kennedy, Ben Taylor and Dr Alessandro Cini. Special thanks to Dr Daisy Taylor whom I consider my bioinformatics mentor, thank you for patience and encouragement and for always having a positive attitude to life, and Dr Michael Bentley and Dr Chris Wyatts who helped me further with the bioinformatics. To the community ecology group: Edith Villa, Tom Timberlake and Nick Tew who kindly adopted me in their hive and baked the best cakes ever. I learned more than I previously knew about insects, plant communities and ecological robustness. To the Mexican community in the School of Biological Sciences which always provided me with advice, wisdom, Mexican food and gave me asylum when I arrived in Bristol: Dora Cano, Edith Villa and Angelica Menchaca. To my family for always supporting me and encouraging me to do what I love. Finally, this work would not have been done without the encouragement of my husband Benjamin Arana who quit his job back in Mexico and joined me on this crazy journey. Thank you for your support, your blind confidence in me, and for your endless abilities as field assistant (2016- 18), chauffeur, bioinformatician, chef, just to mention a few. Like Crazy! iv v I declare that the work in this dissertation was carried out in accordance with the requirements of the University’s Regulation and Code of Practice for Research Degree Programmes and that it has not been submitted for any other academic award. Except where indicated by specific reference in the text, the work is the candidate’s own work. Work done in collaboration with, or with the assistance of, other, is indicated as such. Any views expressed in the dissertation are those of the author. SIGNED: …………………………………………… DATE: …………………….. vi vii Table of Contents Chapter 1: General introduction ........................................................................................ 2 MOLECULAR MECHANISMS OF BEHAVIOURAL TRANSITIONS IN INSECT LIFE CYCLES ....... 3 Phenotypic plasticity ......................................................................................................................... 3 Transitions as examples of phenotypic plasticity ............................................................................. 5 MECHANISMS OF TRANSITIONS ..................................................................................... 7 TRANSITIONS IN INSECTS AS ROUTES TO UNDERSTANDING MECHANISMS OF PHENOTYPIC PLASTICITY ............................................................................................................................... 9 Life-history transitions in plasticity in insects ................................................................................... 9 Evolutionary transitions in plasticity in insects ............................................................................... 11 Behavioural transitions in plasticity in insects ................................................................................ 13 WASPS AS MODELS TO STUDY LIFE-HISTORY AND BEHAVIOURAL TRANSITIONS ........... 15 Simple societies of Polistes wasps as models to study life-history transitions ............................... 16 Ammophilini non-social wasps to study behavioural transitions ................................................... 17 AIMS AND QUESTIONS ADDRESSED IN THIS THESIS ...................................................... 20 Chapter 2 – Molecular basis of a major life-history transition: the shift from worker to queen in simple societies of the social paper wasp, Polistes lanio ............................................................................. 20 Chapter 3 – Molecular basis of an evolutionary transition: testing the ovarian ground plan hypothesis in the non-social sphecid wasp, Ammophila pubescens ........................................................... 21 Chapter 4 – Molecular basis of behavioural transitions: brain transcriptional changes during the nesting cycle of Ammophila pubescens ....................................................................................................... 22 Chapter 5 – Population genetics of Ammophila pubescens and implications for its conservation 22 Chapter 6 General discussion and a conceptual unified model for mechanisms of transitions – reprogramming ...........................................................................................................................................
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