The Dynamics of Reproductive Dominance in Dinosaur Ants
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The Dynamics of Reproductive Dominance in Dinosaur Ants Claire Louise Asher Submitted in accordance with the requirements for the degree of Doctor of Philosophy The University of Leeds School of Biology September 2013 ii Image © Dian Thompson 2013 The candidate confirms that the work submitted is her own and that appropriate credit has been given within the thesis where reference has been made to the work of others. The contribution of the candidate and the other authors to this work has been explicitly indicated below. This copy has been supplied on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement. The right of Claire Asher to be identified as Author of this work has been asserted by her in accordance with the Copyright, Designs and Patents Act 1988. © 2013 The University of Leeds, Claire Asher iii Acknowledgements Professional Acknowledgements I would like to thank the Natural Environment Research Council (NERC) (NE/G012121/1) and the Institute of Zoology, for funding this research. I also thank the Brazilian Government for their help in facilitating the collection and transport of colonies to the UK (transported under permits 10BR004553/DF and 11BR006471/DF from the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais). The work for several chapters of this thesis includes collaborations with Dr Jose O Dantas (JOD), Dr Aline Andrade (AA), Natália Dantas (ND), Luzicleia Sousa (LS), Rafael Figueredo (RF), Benjamin White (BW), Dr Afsaneh Maleki (AfM), Dr Heinz Himmelbaur (HH), Dr Anna Ferrer Salvador (AFS), Dr André Minoche (AnM), Dr Francisco Câmara Ferreira (FCF), Dr Pedro Ferreira (PF) and Dr Anna Vlasova (AV). Their contributions are explicitly detailed below. Chapter Two: JOD assisted in locating and collecting ant colonies in Aracaju. AA, ND, LS and RF assisted in field observations of foraging behaviour, ND also assisted in collection of colonies in Campo Formoso. Chapters Three and Four: JOD assisted in collecting ant colonies in Aracaju. Chapter Five: BW performed some behavioural observations and collected video data. Chapters Six and Seven: HH and AF sequenced DNA and RNA samples, HH, AM and FCF assembled the genome, AM assembled and normalised the transcriptome data. AM and AV performed functional annotation of the transcriptome. My own contributions, fully and explicitly indicated in the thesis, have been as follows. Collecting and transporting ant colonies from Brazil to the UK, as well as set-up and daily care of ant colonies in the UK (all chapters). Nest ecology measurements and behavioural observations of natural foraging in Campo Formoso (chapter two), behavioural observations of aggression (all chapters) and division of labour (chapter three and six) in the laboratory in Aracaju, Leeds and London, as well as statistical iv analyses of these data. All egg policing experiments (chapter five), all RFID set-up and data analysis including developing R code for this task (chapters two and six). Behavourial observations of allogrooming, and statistical analysis of data generated by myself and BW (chapter four). DNA and RNA extractions, including protocol optimisation (chapter six and seven). Statistical analysis of the transcriptome data, BLAST analyses against the Apis mellifera genome, correlational analyses of foraging activity and gene expression (chapter six). Generation and analysis of toolkit list (chapter seven). My supervisors Prof William Hughes and Dr Seirian Sumner have provided feedback on experimental design, data analysis and drafts of all chapters. As a collaborator on this project, Dr Fabio Nascimento provided invaluable assistance during field trips to Brazil. My assessors Dr Lesley Morrell and Dr Keith Hamer gave useful feedback during my 9- month and 2-year vivas. I would like to thank the members of the Hughes and Sumner labs, past and present, for their support, comments and advice throughout my PhD. In no particular order: Rowena Mitchell, Pete Graystock, Dr Crystal Frost, Dr Sophie Evison, Dr Adam Smith, Dr Kat Roberts, Dr Judith Slaa, Dr Paula Chappell, Henry Fergusson-Gow, Thibault Lengronne, Emily Bell, Dr Eli Leadbeater, Dr Inti Pedroso and Dr Ian Warren. In addition, thanks to Dr Kate Cibrowski for her tireless support with optimising laboratory protocols for RNA and DNA extraction. Several informal meetings have also provided feedback on experimental design and data interpretation including the London Social Insect group, and the Behavioural and Population Ecology (BPE) and Evolutionary and Molecular Ecology (EME) theme groups at the Institute of Zoology. Personal Acknowledgements A massive thank you to my family, and particularly my parents, Nick and Jane, for their tireless support, both financial and emotional, throughout my PhD and before. I also owe a huge thank-you to my friends at the Universidade Federal De Sergipe, in particular Fernanda Veira, Hans Kelstrup and Becky Matter and Tiago Santos da Silva, who went out of their way to accommodate me during my fieldwork. I owe a special thanks to Fernanda and her family, who gave me a place to stay and a friend when I v needed one most and who helped me navigate the logistics of fieldwork in Brazil. Likewise, Aline Andrade provided me with a place to stay in Campo Formoso, welcomed me into her home and went way over and above to make sure my trip went well. And Natália Dantas, who stayed with me in a remote field site, dealt with appalling weather and access issues, helped make sure my field work ran as smoothly as possible, and most of all provided companionship during my visit. I also want to thank some of my friends at the University of Leeds and the Institute of Zoology, who I have not already mentioned, for friendship, support and laughter throughout my PhD, in particular Katie Arundel, Clare Duncan, Terri Freemantle, Liz Elliot, Helen Beeston and James Lloyd. I would also like to thank Craig Roscoe, my A-level biology teacher at Newbury College, who inspired me to study biology at university. Finally, some of my oldest friends, for their support and understanding during my fieldwork and PhD as a whole, for skyping with me when I was in the middle of a field, for long chats, and also for putting up with me being a terrible friend during the more stressful parts of this project, thanks to Lynne Shone and Gemma Dodd. You are the best friends anybody could ask for. I would also like to thank Dian Thompson for the front cover image of this thesis. vi Abstract Social insects represent one of the pinnacles of social evolution, and their huge ecological success may be attributable to the sophisticated division of labour and conflict resolution observed in their societies. Eusocial societies exist along a continuum from facultative and primitive (simple) societies in which subordinates retain reproductive totipotency into adulthood, to advanced societies in which the sterile worker caste are committed to their subordinate role. Queenless ponerine ants are unusual, however, exhibiting a simple social structure but having recently diverged from an advanced ancestor. They therefore represent a powerful model system for understanding the roles of evolutionary history, ecology and sociality on behavioural and physiological division of labour. Here, I investigate the influence of reproductive dominance on division of labour and social cohesion in the queenless dinosaur ant, Dinoponera quadriceps. I also present the first description of their natural foraging and nesting ecology. Finally, I investigate the physiological control of division of labour and behavioural plasticity, and explore the relative contribution of conserved and novel genes in the evolution of simple society in this species. Dinosaur ants exhibit remarkable behavioural plasticity despite their advanced ancestry; individual behaviour is strongly influenced by future reproductive prospects and learned aspects of the social environment. They exhibit a discontinuous social hierarchy, in which the reproductive female is transcriptionally distinct from her subordinates, with the largest expressional differences observed in relation to reproductive physiology. Their advanced ancestry is evident both behaviourally and transcriptionally; they exhibit few differences in gene expression within the ancestral worker caste as well as advanced behaviours such as allogrooming, which has been co-opted for a role in social cohesion since their reversion to simple society. Dinosaur ants reveal the relative influences of social behaviour and evolutionary history in shaping the behavioural and physiological characteristics of eusocial societies. vii Table of Contents Acknowledgements ..........................................................................................................iii Abstract............................................................................................................................vi Table of Contents ............................................................................................................vii List of Tables.................................................................................................................... xii List of Figures ................................................................................................................. xiii Chapter 1 Introduction ............................................................................................14 1.1 Overview................................................................................................................14