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Studies of the Spread and Diversity of the Insect Symbiont Arsenophonus Nasoniae

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Studies of the Spread and Diversity of the Insect Symbiont Arsenophonus Nasoniae Studies of the Spread and Diversity of the Insect Symbiont Arsenophonus nasoniae Thesis submitted in accordance with the requirements of the University of Liverpool for the degree of Doctor of Philosophy By Steven R. Parratt September 2013 Abstract: Heritable bacterial endosymbionts are a diverse group of microbes, widespread across insect taxa. They have evolved numerous phenotypes that promote their own persistence through host generations, ranging from beneficial mutualisms to manipulations of their host’s reproduction. These phenotypes are often highly diverse within closely related groups of symbionts and can have profound effects upon their host’s biology. However, the impact of their phenotype on host populations is dependent upon their prevalence, a trait that is highly variable between symbiont strains and the causative factors of which remain enigmatic. In this thesis I address the factors affecting spread and persistence of the male-Killing endosymbiont Arsenophonus nasoniae in populations of its host Nasonia vitripennis. I present a model of A. nasoniae dynamics in which I incorporate the capacity to infectiously transmit as well as direct costs of infection – factors often ignored in treaties on symbiont dynamics. I show that infectious transmission may play a vital role in the epidemiology of otherwise heritable microbes and allows costly symbionts to invade host populations. I then support these conclusions empirically by showing that: a) A. nasoniae exerts a tangible cost to female N. vitripennis it infects, b) it only invades, spreads and persists in populations that allow for both infectious and heritable transmission. I also show that, when allowed to reach high prevalence, male-Killers can have terminal effects upon their host population. Secondly, I examine the phenotypic and genetic differences of a novel strain of Arsenophonus that has recently diverged from the male-Killer following a host-shift event. I show that interspecific transmission can lead to rapid changes in symbiont biology, shifting away from reproductive parasitism and reliance upon mixed transmission towards mutualism, pure heritability and host-specialisation. I also show that these transitions are underpinned by specific genomic diversification. These findings have important implications for the way in which we view symbiont dynamics in nature and predict their outcome in terms of virulence and phenotype evolution. Further, it highlights the rapid directed selection pressures that symbionts are regularly exposed to following a host-shift and how this may be responsible for the diversity seen in nature. 2 Acknowledgements: Writing this thesis would not have been possible without the guidance and support of a few Key individuals. First and foremost I am more than thankful to my supervisors. Firstly, to Greg Hurst for access to his brain, time, and never-ending supply of chocolates over the past four years. His readiness to share his depth of Knowledge, insights into the field, and patience have made this thesis possible. Secondly, a great debt of gratitude is owed to Kayla King. Her infectious enthusiasm for our little corner of science, and her unwavering mentorship have brought me a long way in such a short time. We’re told to expect to hate our supervisors by the end, so you both must have done a terrible job because I think you’re ace. I owe further thanKs to Crystal Frost and Annabel Rice for their support in the later stages of my PhD and a willingness to push wasps when the need arose. Additional thanKs to Alistair Darby who has been more than willing to help with genome exploration and to Anne Lizé, an inspirational force of nature. I also owe more than a few beers (or lemonades) to Daria PastoK, who has unassumingly made everyone’s lab- lives run smoothly, we notice, thanKs. ThanK you to those that proofread chapters: Ewan, Angela and Crystal, and again to Ewan for explaining the finer points of GLM analysis. Chapter 3 would not have been possible without Helena and Caitlin, who photographed many, many wasp wings. Also, a massive thanK you to my friends both in Liverpool and afar, and especially to Sophie. You’re all fantastic and Kept me sane at the darKest times. Finally to my family, after many, many years of support, encouragement and the odd fiscal boost, I can finally get a ‘real job’ - but I won’t. Cheers. 3 Table!of!Contents! Abstract:!..............................................................................................................................!2! Acknowledgements:!........................................................................................................!3! Abbreviations:!...................................................................................................................!7! Glossary!of!Terms:!...........................................................................................................!8! Chapter!1:!............................................................................................................................!9! 1.1!Symbiosis:!..........................................................................................................................!10! 1.2!Heritable!Symbiosis!in!insects!....................................................................................!11! 1.2.1!Discovery!and!Background!..................................................................................................!11! 1.2.2!Primary!Endosymbionts!.......................................................................................................!12! 1.2.3!Secondary!Symbiosis!..............................................................................................................!14! 1.2.4!Reproductive!Parasitism!......................................................................................................!15! 1.2.5!Ecologically!contingent!mutualists!..................................................................................!18! 1.2.6!Dynamics!of!secondary!symbionts!...................................................................................!20! 1.3!Infectious!Transmission!in!symbiont!biology!.......................................................!22! 1.3.1!Horizontal!transmission!on!ecological!timescales!....................................................!23! 1.3.2!Consequences!of!horizontal!transmission!on!ecological!timescales!.................!25! 1.3.3!Summary:!Horizontal!transmission!on!ecological!timescales!..............................!26! 1.4!Overview!of!the!field!and!directions!of!study!........................................................!27! 1.5!The!Arsenophonus/Parasitoid!System!.....................................................................!28! 1.5.1!Arsenophonus*nasoniae!..........................................................................................................!28! 1.5.2!Nasonia*vitripennis!..................................................................................................................!30! 1.5.3!Pachycrepoideus*vindemmiae!..............................................................................................!32! 1.6!Thesis!outline!...................................................................................................................!36! Chapter!2:!.........................................................................................................................!38! 2.1!Introduction!......................................................................................................................!39! 2.1.1!Symbiont!Dynamics!................................................................................................................!39! 2.1.2!Modes!of!horizontal!transmission!....................................................................................!44! 2.1.3!MaleJKiller!dynamics!..............................................................................................................!44! 2.1.4!The!Nasonia/Arsenophonus!system!.................................................................................!45! 2.2!The!Model:!.........................................................................................................................!47! 2.2.1!Incorporating!infectious!transmission!...........................................................................!47! 2.2.2!Incorporating!direct!cost!of!infection!to!offspring!number!...................................!53! 2.3!Results!................................................................................................................................!55! 2.4!Discussion!..........................................................................................................................!60! Chapter!3!..........................................................................................................................!65! 3.1!Introduction!......................................................................................................................!66! 3.1.1!Drive!of!maleJkillers!...............................................................................................................!66! 3.1.2!!Direct!costs/benefits!of!symbiont!carriage!.................................................................!67! 3.1.3!Arsenophonus*/Nasonia*interaction!.................................................................................!68! 3.2!Methods!..............................................................................................................................!70!
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