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Disease Defence in Garden Ants

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Disease Defence in Garden Ants Disease defence in garden ants by Christopher D Pull July, 2017 A thesis presented to the Graduate School of the Institute of Science and Technology Austria, Klosterneuburg, Austria in partial fulfilment of the requirements for the degree of Doctor of Philosophy © By Christopher D Pull, July, 2017 All Rights Reserved I hereby declare that this dissertation is my own work and that it does not contain other people’s work without this being so stated; this thesis does not contain my previous work without this being stated, and the bibliography contains all the literature that I used in writing the dissertation. I declare that this is a true copy of my thesis, including any final revisions, as approved by my thesis committee, and that this thesis has not been submitted for a higher degree to any other university or institution. I certify that any republication of materials presented in this thesis has been approved by the relevant publishers and co-authors. Signature: _______________________ Christopher D Pull September 26, 2017 Abstract Contagious diseases must transmit from infectious to susceptible hosts in order to reproduce. Whilst vectored pathogens can rely on intermediaries to find new hosts for them, many infectious pathogens require close contact or direct interaction between hosts for transmission. Hence, this means that conspecifics are often the main source of infection for most animals and so, in theory, animals should avoid conspecifics to reduce their risk of infection. Of course, in reality animals must interact with one another, as a bare minimum, to mate. However, being social provides many additional benefits and group living has become a taxonomically diverse and widespread trait. How then do social animals overcome the issue of increased disease? Over the last few decades, the social insects (ants, termites and some bees and wasps) have become a model system for studying disease in social animals. On paper, a social insect colony should be particularly susceptible to disease, given that they often contain thousands of potential hosts that are closely related and frequently interact, as well as exhibiting stable environmental conditions that encourage microbial growth. Yet, disease outbreaks appear to be rare and attempts to eradicate pest species using pathogens have failed time and again. Evolutionary biologists investigating this observation have discovered that the reduced disease susceptibility in social insects is, in part, due to collectively performed disease defences of the workers. These defences act like a “social immune system” for the colony, resulting in a per capita decrease in disease, termed social immunity. Our understanding of social immunity, and its importance in relation to the immunological defences of each insect, continues to grow, but there remain many open questions. In this thesis I have studied disease defence in garden ants. In the first data chapter, I use the invasive garden ant, Lasius neglectus, to investigate how colonies mitigate lethal infections and prevent them from spreading systemically. I find that ants have evolved ‘destructive disinfection’ – a behaviour that uses endogenously produced acidic poison to kill diseased brood and to prevent the pathogen from replicating. In the second experimental chapter, I continue to study the use of poison in invasive garden ant colonies, finding that it is sprayed prophylactically within the nest. However, this spraying has negative effects on developing pupae when they have had their cocoons artificially removed. Hence, I suggest that acidic nest sanitation may be maintaining larval cocoon spinning in this species. In the next experimental chapter, I investigated how colony founding black garden ant queens (Lasius niger) prevent disease when a co-foundress dies. I show that ant queens prophylactically perform undertaking behaviours, similar to those performed by the workers in mature nests. When a co-foundress was infected, these undertaking behaviours improved the survival of the healthy queen. In the final data chapter, I explored how immunocompetence (measured as antifungal activity) changes as incipient black garden ant colonies grow and mature, from the solitary queen phase to colonies with several hundred workers. Queen and worker antifungal activity varied throughout this time period, but despite social immunity, did not decrease as colonies matured. In addition to the above data chapters, this thesis includes two co-authored reviews. In the first, we examine the state of the art in the field of social immunity and how it might develop in the future. In the second, we identify several challenges and open questions in the study of disease defence in animals. We highlight how social insects offer a unique model to tackle some of these problems, as disease defence can be studied from the cell to the society. v Acknowledgments Moving to Vienna and conducting a PhD thesis has been extraordinary. I still sometimes cannot believe that I took the leap and I suspect I will look back on my time in Austria with astonishment. During my PhD I have learnt so many things about ants, science and schnitzel from so many wonderful people, and I am sure to forget a few in saying Vielen Dank to them here. Firstly though, I must thank the people back home, my friends and family, who were extremely supportive in sending me off with my bags packed, and for keeping in contact and welcoming me home with open arms. In particular, I must single out my Mum and Dad, who have always given me the freedom and encouragement to pursue my passions (who can forget the bedroom so full of stick insects we had to take the doors of the wardrobes to fit more in?). On that note, I must also thank my Grandparents, on both sides, for the same reason. Arriving at IST seemed daunting but I was immediately made to feel welcome and, despite not speaking a lick of German, I never felt excluded. I am very thankful to the entire group in those early years, and in particular to Miriam, Line and Matthias, who got me started and were always happy to help whenever I had questions. As the group has grown and changed over the years, I have had the pleasure of working with a diversity of people from different cultures and backgrounds. Thanks (in random order) to Hias, Flo, Anna, Leila, Eva and all the Barbaras, for broadening the mind of this Engländer. You guys were one of the best things about working at IST and I cannot thank you enough for your support during this time. I have been supremely spoilt to work in a lab with such good resources and I must thank the wonderful Cremer group technicians, Anna, Barbara, Eva and Florian, for all of their help and keeping the lab up and running. You guys will probably be the most missed once I realise just how much work you have been saving me! For the same reason, I must say a big Dziękuję Ci to Wonder Woman Wanda, for her tireless efforts feeding my colonies and cranking out thousands of petri dishes and sugar tubes. Again, you will be sorely missed now that I will have to take this task on myself. Of course, I will be eternally indebted to Prof. Sylvia Cremer for taking me under her wing and being a constant source of guidance and inspiration. You have given me the perfect balance of independence and supervision. I cannot thank you enough for creating such a great working environment and allowing me the freedom to follow my own research questions. I have had so many exceptional opportunities – attending and presenting at conferences all over the world, inviting me to write the ARE with you, going to workshops in Panama and Switzerland, and even organising our own PhD course – that I often think I must have had the best PhD in the world. You have taught me so much and made me a scientist. I sincerely hope we get the chance to work together again in the future. Thank you for everything. I must also thank my PhD Committee, Daria Siekhaus and Jacobus “Koos” Boomsma, for being very supportive throughout the duration of my PhD, and I look forward to our little tête-à-tête in July! Lastly, my greatest thank you goes to my partner, Tom Ikonen. Somehow we have survived what, at often times, felt like an ordeal, and I still cannot believe that is almost over. You have helped me keep perspective on what is important and I am so excited to start the chapter of our lives – finally – together. Thank you! vi About the Author Christopher D. Pull completed a BSc in Zoology and an MSc in Biological Sciences Research at Royal Holloway University of London, before joining IST Austria in August 2012. His main research interests are animal behaviour and the evolution of sociality. Specifically, Christopher’s research has focussed on disease in social animals, using ants and bees as study organisms. During his PhD, Christopher has presented his research at many international conferences, such as the European IUSSI conference in Helsinki, Finland in 2016, and attended several workshops, including the 2013 Tropical Behaviour, Ecology and Evolution field course in Gamboa, Panama and the 2014 Evolutionary Biology workshop in Guarda, Switzerland. In addition, Christopher created and organised a PhD course for international students studying social evolution, hosted by IST Austria in 2016. vii List of Publications Appearing in Thesis 1. Pull CD, Ugelvig L V, Wiesenhofer F, Tragust S, Schmitt T, Brown MJF, Cremer S. 2017 Destructive disinfection of infected brood prevents systemic disease spread in ant colonies. bioRxiv (doi:10.1101/116657) 2. Cremer S, Pull CD, Fürst MA. 2018 Social immunity: emergence and evolution of colony-level disease protection. Annu Rev Entomol (doi:10.1146/annurev-ento- 020117-043110) 3.
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