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1 Theoretical Aspects of the Evolution of Reproductive Parasites by Jan Engelstaedter A thesis submitted for the degree of Doctor of Philosophy of the University of London December 2006 Department of Biology University College London UMI Number: U592750 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a complete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. Dissertation Publishing UMI U592750 Published by ProQuest LLC 2013. Copyright in the Dissertation held by the Author. Microform Edition © ProQuest LLC. All rights reserved. This work is protected against unauthorized copying under Title 17, United States Code. ProQuest LLC 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106-1346 2 Declaration This dissertation represents, except where specifically mentioned in the text, the results of my own research. The dissertation is not substantially the same as any that I have submitted for a degree or other qualification at this or any other university. No part of my dissertation has already been or is currently submitted for any such degree or other qualification. Jan Engelstaedter Dr. Gregory Hurst teandidate Supervisor 3 A bstract Reproductive parasites are maternally inherited endosymbionts that manipulate the reproduction of their hosts in a way that enhances the transmission of the parasites, but is deleterious to the hosts. In the present thesis, I try to resolve some ques­ tions concerning the evolution of reproductive parasites and their hosts by means of theoretical modelling, using a variety of approaches including recurrence equations, optimisation, and stochastic modelling. I first study the question: ’Can male-killing bacteria and meiotic drive elements influence each others’ spread and equilibrium frequency in a population?’ and demonstrate they can. Following this, I examine two questions with respect to host evolution. First, can male-killing or Cl-inducing bacteria facilitate the evolution of haplodiploidy? I conclude that past work on this has been overoptimistic, but that the process is possible. Second, how does the pres­ ence of male-killing bacteria affect basic population genetic processes, in particular the interplay between natural selection and random genetic drift? I demonstrate that the host population behaves approximately as if only uninfected individuals existed. I then examine two questions in relation to endosymbiont biology. First, what is the impact of mating systems and segregation on the evolution of new Cl-types? I propose outbreeding systems as a context where new Cl-types can evolve. Second, how can we expect selection to act on two bacterial strains of reproductive parasites in doubly infected hosts with respect to their density? Finally, I examine how we expect the incidence of reproductive parasites to vary in time within a host clade, and how the phylogenetic history of the host clade affects the pattern of spread and expected incidence of the parasites. I conclude my thesis with a general overview of what is known about the evolution of reproductive parasites both empirically and theoretically, and outline some promising future avenues of research. 4 Acknowledgments First and foremost, I would like to thank my supervisor Greg Hurst for having me as his student and for his excellent supervision. Thanks a lot for giving me all the freedom in my research I could have wished for, for preventing my mathematics from taking off from firm biological ground, for untiring battles with my germanic laden manuscripts and for unwholesome amounts of chocolate and gin. This PhD project would not have been possible without a Graduate School Re­ search Scholarship from University College London. I would also like to acknowledge financial support from the Genetics Society and the NSF for attending the 4th Inter­ national Wolbachia Conference. I was very lucky to be part of a decidedly friendly and cooperative group. Horacio taught me much about Drosophila and conceived the project detailed in Chapter 2. Max helped me to see a lot of things more clearly through many discussions on several aspects of this thesis. Zoe opened my eyes for the difficulties of cross-disciplinary communication. Sylvain, although based on the opposite side of the globe, has greatly improved this thesis by many discussions and comments, especially on Chapter 5. Olivier shared with me his results concerning the odd Culex Wolbachia system. Emily and Tim were great room mates and helped me with many small things. I am sure that Kate would have helped me a lot as well, if she had not started her PhD when I was about to leave. Thanks a lot to all of you! For help with various issues, I am also grateful to the faculty of the Biology Department, in particular my second supervisor Prof. Andrew Pomiankowski (who also contributed ideas to Chapter 5), Dr. Kevin Fowler and Prof. Jim Mallet. Many thanks to Ian Evans, Jacques Gianino and Dave Turner for always being very helpful with the administrative side of things. Many people outside UCL improved my thesis through discussions or comments, among them John Jaenike, Benjamin Normark, Tine Huse, Francis Jiggins, Kelly Dyer, Kirsten Hilgenbrocker and Matthias Flor. By forcing me to explain my thoughts clearly and convincingly, Peter Hammerstein was of great help to me to get on with Chapter 6. Arndt Telschow provided plentiful of comments on several chapters, and I am also very grateful to him for his help and support in Japan. 5 One of the best things about my time in London was that I gained great friends from all around the world, many thanks to all of you! To Lorenzo, for the Italian coffee, the expeditions into the cultural heart of London and innumerable discussions about love and science. To Barbara, for her support in difficult times, for always making me feel relaxed and for the best mousse au chocolat I ever had. To Marie, for good pub nights, for enriching my life with Toe and for a wonderful time in Marseille. To Imogen, for making me feel ashamed of my English and for dragging me from Wolfson House into London’s most hidden Jazz clubs. To Lucia, for all her fruitless attempts to teach me some Spanish and for lots of hot chocolates. To Caspar, Imma, Julia, Kat and Loli, my friends and flatmates in Haringey; despite the livestock, I will miss ’our’ kitchen very much! Wolfson House and the Bree Louise would not have been the same without the sovereigns and subjects of the Stalkie-Empire: Martin, Dave, Ellen, Laura, Sam, Ian and Jen, thanks a lot to all of you! The same applies to our yeasty lab neighbours Duncan and Callum. Thanks also to all the other nice people I met at UCL, including Ana, Nathalie, Sarah, Liqin, Edd and Kate. Many thanks are also due to Tina, Danny, Alex, Kathi, Jo, Beate, Nico, Kathi and Christoph, my friends in Berlin, for making returns to my home town enjoyable and for stipulating wonderful trips in England while visiting me. Thanks a lot to Kogo for the nice evenings we had in Kyoto and Osaka. I am very much indebted to my parents, who have always supported my scientific career and who provided a perfectly quiet and convenient refuge for the last few weeks of writing this thesis. My sister Julia was always there for me, except for the few occasions when she was off to Hawaii. Finally, many thanks to Nga; you gave me so much. Contents 1 Introduction 17 1.1 Background ................................................................................................... 18 1.1.1 Parasites and vertical transmission .............................................. 18 1.1.2 Genetic conflict and selfish genetic e le m e n ts .............................. 20 1.1.3 Reproductive p a ra site s .................................................................... 21 1.2 W olbachia ....................................................................................................... 23 1.2.1 Brief history of Wolbachia re se a rc h .............................................. 23 1.2.2 Biology of W olbachia ....................................................................... 24 1.2.3 Distribution of W olbachia .............................................................. 24 1.2.4 Phylogeny and systematics of W olbachia ...................................... 25 1.2.5 Wolbachia genom es ........................................................................... 27 1.3 Other reproductive parasites ...................................................................... 29 1.3.1 R ic k e ttsia ........................................................................................... 29 1.3.2 Arsenophonus.................................................................................... 29 1.3.3 Spiroplasma........................................................................................ 30 1.3.4 Cardinium ........................................................................................... 30 1.3.5 F lavobacteria ..................................................................................... 31 1.3.6 M icrosporidia ..................................................................................... 31 1.4 Phenotypes of reproductive parasites ...................................................... 33 1.4.1 Feminisation ........................................................................................ 33 1.4.2 Induction of
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