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Investigating the Relationship Between Gut Microbiota and Animal Behaviour

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Investigating the Relationship Between Gut Microbiota and Animal Behaviour 1 Investigating the relationship between gut microbiota and animal behaviour Thesis submitted in accordance with the requirements of the University of Liverpool for the degree of Doctor in Philosophy by Chloe Elizabeth Heys. June 2018 2 Abstract: Investigating the relationship between gut microbiota and animal behaviour Chloe Elizabeth Heys An individual’s gut microbiota is increasingly recognised as having a key role in many host behaviours. In insects, the environment largely determines the host gut microbiota, with the majority ingested through the diet. In this thesis, I examine a series of host-gut microbiota relationships within three species of Drosophila with varied ecologies. Initially, I analyse the current methods used to eliminate the gut microbiota in Drosophila melanogaster, key to studying host-microbiota relationships and providing a foundation for this thesis. I then use this information to assess the role of the gut microbiota as an honest signal in age-based mate choice in Drosophila pseduoobscura. Finally, I examine the role the gut microbiota plays in specialisation in Drosophila sechellia, through adaptation to its toxic host plant, Morinda citrifolia. To attribute a specific behaviour to the gut microbiota, it must first be removed. However, removal can have serious physiological side effects on the host organism, and the most effective and least detrimental method of doing this is widely debated. I analyse commonly used methods of removing the gut microbiota in Drosophila melanogaster and find the addition of low- dose streptomycin to the dietary media is more effective and has fewer physiological effects than other methods such as egg dechorionation or rearing on a sterile diet. Female Drosophila pseudoobscura are known to discriminate between males based on age. This may occur through the alteration of the cuticular hydrocarbon (CHC) profile of males, which can alter due to a varied gut microbiota caused by a varied diet. I determine that the gut microbiota influences female preference for older males and is a key component of attractiveness to females. I examine the role of the gut microbiota in Drosophila sechellia, in adaptation to its toxic host plant, Morinda citrifolia, and characterise the gut microbiota of this Drosophilid species for the first time. Rearing flies on M. citrifolia, a standard laboratory diet, and an additional salak (Salacca zalacca) fruit that lacks the toxic compounds present in M. citrifolia, I find that flies reared on a laboratory diet have a significantly reduced weight. However, there is no impact on development time or subsequent mating behaviours when compared to individuals reared on the wild, M. citrifolia diet. Finally, by creating experimental evolution lines of D. melanogaster supplemented with D. sechellia gut microbiota, I disentangle the role of pH in shaping the gut microbiota from the co-evolution of the gut microbiota within D. sechellia. D. melanogaster are highly averse to the scent of octanoic acid, the main toxic constituent within M. citrifolia, whereas D. sechellia are highly attracted. After ten generations D. melanogaster show significantly less aversity to octanoic acid. I determine that Lactobacillus plantarum acts as a detoxifying agent by metabolising octanoic acid, therefore suggesting this 3 bacterium has been fundamental to the ecological transition and specialisation of D. sechellia. Taken together, the chapters of this thesis further uncover the role of host- microbiota interactions in important ecological and evolutionary processes within Drosophila, from elucidating a principle method in gut microbiota research, to underlying mate choice mechanisms and finally to dietary specialisation. 4 Acknowledgements It’s hard to know where to begin when writing this acknowledgement section. I’m very fortunate to have a lot of close friends and family in my life, so this section is at risk of rambling on like an Oscar’s acceptance speech no-one really wants to hear. I think my first and foremost thanks must go to Zen. Without a doubt, she has been the best supervisor I could have ever asked for. I had never thought about studying for a PhD before, until I was fortunate enough to be supervised by her during my Undergraduate honours project. Her passion and dedication for research inspired and enthused me to pursue my own research path, and she has been there every step of the way. She has read every piece of work I’ve ever written and offered endless support when things go wrong. She has even listened to my many chicken (and now turkey!) stories I’ve distracted her with over the years. We’ve been working together for a long time now and I’ll miss that very much. My honorary supervisor, Anne Lizé, also deserves a tremendous thank you. I’ve known Anne almost as long as I’ve known Zen, and she has provided support and essential feedback this entire journey, even from afar. Our skype sessions have been invaluable and I’m very proud of the work we have completed together. Thanks also to Al Darby for filling the gap in my knowledge regarding host-microbiota interactions. His contribution has greatly strengthened this thesis. Further thanks to Fran Blow who took time out of her own busy schedule to teach me everything she knows about microbiology! Thanks must also go to my internal assessors, Iain Young and Greg Hurst, whose constructive comments have helped shape this thesis enormously. Thank you to everyone at the University of Liverpool sports centre, where I have wiled away many, many hours over the past few years. Having a friendly place where I can go to switch off my brain for a while has helped retain my sanity. Special thanks in particular must go to Inigo, head coach of 5 our little boxing club, and the rest of the boxing crew. Thanks for allowing me to punch you! To all my friends who have supported me over the years, even the ones who have no idea what I am actually doing, thank you for listening to me tell you about fruit flies. In particular, Adam Fisher for providing stats advice even at very short notice, and Amy Eacock and Becky Jones, for letting me distract you from your own work and providing first-class dog sitting services. Amy, tin-foil ball will forever live on. Chapters four and five of this thesis would not have been possible without Matthew and Claire Heys. After my Morinda citrifolia suppliers up and moved nurseries, I found myself stranded part-way through experiments with no fruit to feed my Drosophila. After complaining to Matthew and Claire about this situation, Matthew contacted a work colleague in Malaysia and Claire a friend who was on holiday in Thailand. Between them I ended up with enough fruit to sustain my experiments and beyond! I cannot thank my parents enough for everything they have done for me. They have provided both emotional and financial support for the many years I’ve spent at University and beyond. The annual trip to Australia consisting of copious amounts of shopping with my Mum was always a much-needed break. My Dad has also read every piece of work I’ve submitted - his proof- reading skills are second to none! I’m excited to (hopefully) become the first Dr Heys in the family! Finally, I definitely would not have been able to complete this PhD without Patrick. I feel like I’ve been quite calm throughout this thesis-writing process, but I’m sure the opposite is true, so thanks for putting up with me without complaint! He has always encouraged and supported me. Thank you for making sure I always take time-out to stroll along the beach together with the dogs. I’ll conclude this section with the insightful words of my dear friend, Ellie Watts: “when faced with a difficult decision, one must always trust your gut.” 6 Table of contents 1.Chapter One: General Introduction........................................................10 1.1 The ecology and evolution of host-microbe interactions....................10 1.1.1 Microbiota and behaviour in insects..........................................13 1.2 The Drosophila microbiota................................................................15 1.3 The Drosophila gut............................................................................19 1.3.1 Drosophila gut structure............................................................19 1.3.2 Drosophila gut microbiota..........................................................22 1.4 Outline of this thesis.........................................................................25 2. Chapter Two: The effect of gut microbiota elimination in Drosophila melanogaster: A how-to guide for host-microbiota studies...................29 2.1. Abstract.............................................................................................29 2.2 Introduction.........................................................................................30 2.3 Materials and Methods.......................................................................33 2.3.1 Fly stocks...................................................................................33 2.3.2 Experimental treatments............................................................34 2.3.3 Physiological assays.................................................................35 2.3.4 Bacterial analysis.......................................................................38 2.3.5 Statistical analysis.....................................................................39 2.4 Results...............................................................................................40
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