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Cognitive Mechanisms Underlying Responses to Sperm Competition in Drosophila Melanogaster

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Cognitive Mechanisms Underlying Responses to Sperm Competition in Drosophila Melanogaster Cognitive mechanisms underlying responses to sperm competition in Drosophila melanogaster James Luke Rouse Submitted in accordance with the requirements for the degree of Doctor of Philosophy The University of Leeds School of Biology November 2016 The candidate confirms that the work submitted is his/her own, except where work which has formed part of jointly-authored publications has been included. The contribution of the candidate and the other authors to this work has been explicitly indicated below. The candidate confirms that appropriate credit has been given within the thesis where reference has been made to the work of others. Jointly authored publications Rouse, J. Bretman, A. (2016) Exposure time to rivals and sensory cues affect how quickly males respond to changes in sperm competition threat, Animal Behaviour, 122, 1-8 All experimental work was carried out by the author of this thesis; manuscript preparation was jointly shared between the authors 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. © 2016 The University of Leeds and James Luke Rouse ii Acknowledgments I doubt many people will read this Thesis too closely, but from personal experience I know the acknowledgments are scrutinised, so I better make them good. First and foremost, I would like to thank my supervisor Amanda for providing me with the opportunity to perform this work. From helping me understand statistics as a baby-faced undergraduate she has encouraged and cajoled me to the baby-faced 24 year old I am today. I couldn’t have asked for a better supervisor. I am also grateful to Tracey Chapman, who started me working on Drosophila, Tom Price for fly lines, Elwyn Isaac as my secondary supervisor and John Altringham as my assessor. I also wish to thank Grace Hoysted, Steve Laird and Liz Duncan for their help in unravelling the qPCR knots in my head and Zatul and Petra who have provided advice on fly lines. I am lucky to have taught and worked alongside some very good undergraduate and Master’s Students who have helped collect some of the data in this thesis. Katherine Watkinson, Luke Evans, Alice Gooch and Laura Tyndall, I hope I haven’t scared you away from science forever. I would particularly like to thank the people who have had to share a lab with me throughout some of these 3 years, Tom Leech and Laurin McDowall both have been extremely helpful and a source of constant support throughout the process. I would particularly like to apologise to Laurin for making her collect data in a dark cupboard for hours at a time. Throughout my 3 years here I have met many people who have been brilliant. I want to particularly thank Roger, my fellow tiny ginger impersonator (cooookkkkkkiiiieee). Double A-ron, the man who taught me about flat décor (sort of). Charlotte Hopkins and Jamie and Claire, my PhD Mum and Dad. I would also like to thank Michael iii Norman, for being my drinking partner whenever we actually manage to meet up, and all the office folk who have had to view the atrocity that is my desk. To my family, especially Mum and Dad, I don’t think I would be able to remember why I went to Leeds University every day if not for your continued questions, specifically the classic “so what are you doing again?” Also a shout out to my brother Edward, who has found hours of amusement in the fact I work on fly sex and has taken advantage with various witty birthday mugs. You’ll have to find me a different present this year. Last, but definitely not least I would like to thank Ruth Norman. She has kept me fed, focussed my mind, introduced me to cycling and provided a focal point for much of my craziness throughout the last two years, even though she herself has been doing a PhD. The whole thing would have been much less fun without you. iv Abstract In this thesis I use Drosophila melanogaster as a model organism to study the possible cognitive mechanisms controlling plastic behavioural responses to sperm competition. This plastic behaviour involves a male D. melanogaster responding to the presence of a rival male by increasing mating duration when housed with a female. I provide a general context to the work (Chapter 1) before examining my model in more temporal detail by investigating how the length of time males were exposed to a high sperm competition environment affected maintenance time of the plastic behaviour. I show that for males to accurately portray the sperm competition environment in their behaviour over a useful timescale they must possess accurate sensory systems. Without these, behaviour is still fully plastic, but change occurs at a slower speed than males with full sensory ability (Chapter 3). I then show that extended mating duration is controlled by a suite of well-known learning and memory genes highlighting the need for specific memory pathways to reflect ecological change (Chapter 4). However, those same genes do not change in their expression due to increased sperm competition, potentially pointing to some other mechanism of temporal change underlying the behavioural change (Chapter 5). Due to this reliance on learning and memory, I show that an increase in sperm competition can affect cognitive ability, and increase expression of synaptic genes over a longer time period (Chapter 6). Finally, I summarise my thesis findings and discuss how future research can build on the research presented to develop the field (Chapter 7). My research shows that learning and memory is paramount for males to react to changes in the sperm competition environment on a relevant timescale where behaviour and the environment have not become mismatched. In addition, I show that sperm competition pressures can cause an increase in male individual v cognitive ability, posing the question of whether competition is one of the main drivers of non-mammalian cognitive ability. vi Table of contents Acknowledgements .................................................................................. iii Abstract ......................................................................................................v Commonly used Abbreviations ................................................................ vi Table of Contents ..................................................................................... vii List of Figures .......................................................................................... xv List of Tables ......................................................................................... xviii Chapter 1. General Introduction ...............................................................1 1.1 Phenotypic plasticity ................................................................. 2 1.1.1 How do different types of plasticity evolve? .................. 3 1.2 Behavioural plasticity ................................................................ 3 1.2.1 Cost of behavioural plasticity ......................................... 6 1.2.2 Behavioural plasticity and cognition .............................. 7 1.3 Role of social environment in driving cognition ..................... 8 1.4 Sperm competition .................................................................. 10 1.5 Sperm competition responses to rival males ........................ 13 1.6 Learning and memory in plastic behaviour ........................... 14 1.6.1 Non-associative learning ............................................... 15 1.6.2 Associative learning ...................................................... 15 1.6.3 Operant conditioning ..................................................... 16 1.7 Memory and plastic behaviour ............................................... 16 1.8 The study system..................................................................... 17 1.8.1 Socially induced extended mating duration ................. 17 vii 1.8.2 Sensory cues involved in extended mating duration .. 18 1.8.3 Lifetime costs and benefits of extended mating duration ......................................................................................... 19 1.8.4 Types of learning in D. melanogaster ........................... 19 1.8.4.1 Associative learning .............................................. 19 1.8.4.2 Courtship suppression .......................................... 22 1.8.5 Genetics of learning and memory in courtship suppression and associative learning .......................... 23 1.8.6 Neuroanatomy associated with associative learning .. 26 1.9 Outline of thesis ....................................................................... 29 Chapter 2. Maintenance of extended mating duration in response to sperm competition threat is determined by exposure time to rival males 2.1 Summary .................................................................................. 32 2.2 Introduction .............................................................................. 33 2.3 Materials and methods ............................................................ 35 2.3.1 General experimental set-up ......................................... 35 2.3.2 Maintenance of the response after 72h exposure ........ 39 2.3.3 Effect of exposure time on maintenance time.............. 39 2.3.4 Statistical analysis ......................................................... 39 2.4 Results ...................................................................................... 40 2.4.1 Maintenance of the response after 72h exposure ........ 40 2.4.2 Effect of exposure time
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