HOST SPECIFICITY AND LOCAL ADAPTATION IN GYRODACTYLID S Tracey Anne King This thesis is submitted for the degree of Doctor of Philosophy School of Biosciences, Cardiff University November 2008 UMI Number: U585162 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 U585162 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 DECLARATION This work has not previously been accepted in substance for any degree and is not concurrently submitted in candidature for any degree. Signed . (candidate) Date .fb./.I./.^.QQ1^? ................... STATEMENT 1 This thesis is being submitted in partial fulfillment of the requirements for the degree of PhD. Signed . (candidate) Date . .4ti. / ................ STATEMENT 2 This thesis is the result of my own independent work/investigation, except where otherwise stated. Other sources are acknowledged by explicit references. Signed .. (candidate) Date STATEMENT 3 I hereby give consent for my thesis, if accepted, to be available for photocopying and for inter- library loan, and for the title and summary to be made available to outside organisations. Signed .. (candidate) Date . fit*. /.!. ? l. STATEMENT 4: PREVIOUSLY APPROVED BAR ON ACCESS I hereby give consent for my thesis, if accepted, to be available for photocopying and for inter- library loans after expiry of a bar on access previously approved by the Graduate Development Committee. Signed . (candidate) Date . .4b / J. 7.5vQ Q .^ ......... II ABSTRACT The monogenean fish ectoparasites, Gyrodactylus spp. have been studied extensively as model organisms, but two key areas, to date, have received little attention; host specificity and local adaptation, and these form the central theme of this thesis. Host specificity was examined for two tropical parasite species infecting the guppy; Gyrodactylus turnbulli and G. bullatarudis. Contrary to the expectation that G. turnbulli is a strict specialist, this parasite can infect a range of hosts under both laboratory and semi-natural conditions. Furthermore, the congener species, G. bullatarudis, can infect and reproduce on a temperate fish host, the three-spined stickleback. This thesis also identified different transmission strategies of these two species, which are affected by temperature. Whereas G. turnbulli migrates away from a dead host at high burdens, G. bullatarudis stays with a dead host, even though survival times for both species are similar. Arising from these host specificity studies was the discovery that G. lomi, a parasite of chub, could persist as long-term infections on isolated fish, and two new gyrodactylid species, G. zebrae n. sp. and G. danio n. sp., are described from zebrafish. Finally, local adaptation theory was examined for G. gasterostei , which infects the three-spined stickleback throughout England and Wales but not in the Hebridean Islands. This study ascertained that Hebridean host populations were no more susceptible to G. gasterostei than their mainland counterparts. No evidence of local adaptation was found due to overriding temporal effects. However, local differentiation between populations in their susceptibility and resistance was detected, together with sticklebacks having a much longer immunological memory than previously considered. Ill ACKNOWLEDGEMENTS Firstly, I would like to thank my supervisor, Dr Jo Cable (Cardiff University), for her continuous encouragement, advice, comments and support throughout the course of my PhD. I would also like to thank my external supervisor, Dr Phil Harris (University of Nottingham) for his input and comments on Chapters 6 to 8. Furthermore, I would like to thank Dr Cock van Oosterhout (University of Hull) for his statistical advice and comments on Chapters 3 to 5. I would also like to thank the many people who have helped me throughout my PhD such as David Harris and Dr Iain Barber (University of Leicester) for their assistance in the collection and advice on maintenance of sticklebacks. Susie Coyle and Professor Felicity Huntingford (University of Glasgow) for providing sticklebacks from the Outer Hebrides (Fada and Grogary) and particularly, Dr Andy Shinn (University of Stirling) for his assistance in the collection of sticklebacks from the Howietown trout farm and for the subsequent use of his facilities at the University of Stirling, which enabled their safe arrival at Cardiff. Also, Dr Helen Rodd for her kind permission in citing her for Chapter 2; to Dr Hannu Makinen (University of Finland) and Drs Alison Bell and Ripan Malhi for their generosity in giving access to their stickleback sequences. In addition, to past final year undergraduate students Hayley Upham and Kate Davidson for helping with experimental work and Jenni Lawton for her support, also Mike and Clive from JBIOS and to Hagen, Kordon and staff at Atlantis Aquatics for providing aquarium equipment. I would also like to thank the members of Professor Mike Bruford’s and Dr Jo Cable’s labs for their help and advice and to the Natural Environment Research Council who funded my studentship. Finally and most importantly, I would like to thank my husband, Graham, for keeping me company in the lab in the evenings and weekends, cleaning out fish tanks, acting as scribe and fieldwork assistant hauling me out of muddy ditches and providing tea and chocolate when it was needed most. IV TABLE OF CONTENTS Title Page........................................................................................................................I Declaration ..................................................................................................................... II Abstract.......................................................................................................................... Ill Acknowledgements ....................................................................................................... IV Table of Contents ........................................................................................................... V-VIII List of Tables................................................................................................................. IX List of Figures................................................................................................................X-XIV CHAPTER 1: INTRODUCTION 1.1 GYRODACTYLUS 1.1.1 Overview............................................................................................... 1 1.1.2 Taxonomy ............................................................................................. 1-3 1.1.3 Morphology.......................................................................................... 3-4 1.1.4 Molecular. .............................................................................................4-6 1.1.5 Reproduction ........................................................................................ 6-9 1.1.6 Immunity 1.1.6(i) Innate immunity. ...................................................................9-10 1.1.6(ii) Acquired immunity. ..............................................................10-11 1.1.7 Transmission ........................................................................................ 11-12 1.1.8 Epidemiology ....................................................................................... 12 1.1.8(i) Temperature ..........................................................................12-14 1.1.8(h) Water chemistry. ...................................................................15-16 1.1.8(iii) Pollutants. ..............................................................................16 1.2 HOST SPECIFICITY 1.2.1 Overview...............................................................................................16-17 1.2.2 Defining and measuring host specificity .............................................17-18 1.2.3 What are the mechanisms controlling host specificity? .....................18-19 1.2.4 Specialists vs. Generalists - What is the evolutionary advantage?.... 19-21 1.2.5 Speciation ..............................................................................................21 1.2.6 Monogenean host specificity .............................................................. 21 -23 1.3 LOCAL ADAPTATION 1.3.1 Overview.............................................................................................. 23 1.3.2 When should local adaptation occur? .................................................23-25 1.3.3 Local adaptation and glacial refugia ................................................ 25 1.3.4 Empirical testing and measuring of local adaptation ........................25-26 1.4 MODEL ORGANISMS 1.4.1 Poeciliid -Gyrodactylus turnbulli and G. bullatarudis....................... 26-28 1.4.2 Gasterosteus aculeatus-Gyrodactylus gasterostei.............................28-29 1.5 THESIS AIMS AND LAYOUT.......................................................................30 1.6 REFERENCES............................... ..................................................................