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Evolutionary and Conservation Genetics of the Seychelles Warbler ( Acrocephalus Sechellensis )

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Evolutionary and conservation genetics of the Seychelles warbler ( Acrocephalus sechellensis ) David John Wright A thesis submitted for the degree of Doctor of Philosophy School of Biological Sciences University of East Anglia, UK May 2014 © This copy of the thesis has been supplied on condition that anyone who consults it is understood to recognise that its copyright rests with the author and that use of any information derived there from must be in accordance with current UK Copyright Law. In addition, any quotation or extract must include full attribution. This thesis is dedicated to Laura, my wife and partner-in-crime, for the endless supply of love, support, tea and cake. ii Abstract In this thesis, I investigated how evolutionary forces and conservation action interact to shape neutral and adaptive genetic variation within and among populations. To accomplish this, I studied an island species, the Seychelles warbler (Acrocephalus sechellensis ), with microsatellite markers and major histocompatibility complex (MHC) genes as measures of neutral and adaptive variation respectively. First, I used museum DNA and historical records to reveal a recent bottleneck that provides context for the contemporary genetic variation observed in this species. I then determined the impact of four translocations on genetic diversity over two decades. I found that diversity does not differ significantly between islands but the use of smaller founder sizes in two translocations has caused population divergence. These results indicate that stochastic genetic capture is important in translocations and that future assisted gene flow between populations may be necessary. As a tool for conservation practitioners, I wrote a technical report of the most recent translocation - to Frégate Island - detailing practicalities and outcomes to help inform future translocation policy. Using two translocation events as experiments, I then tested whether MHC-based social mate choice acts to maintain MHC diversity in the Seychelles warbler, finding that male age and heterozygosity, but not MHC, predicted pairing success. Lastly, I investigated survival and reproductive consequences of Ase-ua4 , an MHC class I allele previously shown to confer a survival advantage in the Seychelles warbler. I found widespread patterns of allele frequency increase within cohorts consistent with the survival effect, but no overall increase in population allele frequency over time. I investigated potential antagonistic reproductive mechanisms, but found no clear evidence for why this allele is not driven towards fixation. Collectively, my results provide an interesting case study of the evolutionary conservation approach, whilst providing insight into the importance of maintaining genetic variation in natural populations. iii Acknowledgements I start by giving my sincere thanks to David Richardson for your guidance, friendship and patience through this PhD. Nigel Collar, thank you for the endless positivity and for being my grammar-guru (should that even have a hyphen?!). You two make a great supervisory team! A special thank you to Lewis Spurgin and Karl Phillips – you always had open doors and informative answers to soothe my analytical troubles. I owe my R capabilities to you both. Jenny Gill and John Ewen, thank you for being my examiners. I genuinely enjoyed the viva and appreciated your input. I would also like to thank my funders: the Natural Environment Research Council (NERC) and BirdLife International, for financing my research and I. Cheers! They say a PhD is a lonely business, but that can’t possibly be true when you have ‘team warbler’ with you all the way! Terry Burke and Jan Komdeur, thank you for the biannual injections of fresh ideas and enthusiasm (and for keeping David in order!). Thank you to all Seychelles Warbler Project members past and present; this PhD would simply not have been possible without your collective efforts. Particular thanks to Bebbers, Danni G, Elliemoo, Emma, Fronk, Hannah D, Hannah E, Jildou, Kathryn, Laura, Lewis, Marco, Margarete, Martijn, Michaela, Niki, Owen, Sjouke and Violet. Maybe next time we can think of an easier excuse for tropical adventures…preferably without the dreaded ‘dataface’? Sjouke and Martijn – being trapped on a tiny island with you two is something I’ll never forget…no matter how hard I try! Laura, Hannah – let’s drive the boat ourselves next time! To all at UEA, thanks for putting up with me for these past few years! Particular thanks to Alicia, Aly, Amanda, Amy, Bebbers, Chris, Clare, Claudia, Cock, Conrad, Damian, Danni G, Dave C, Edd, Elizabeth, Elli, Elliemoo, Emma, Helena, Iain, Jacob, Jenny G, Karl, Kitson, Lewis, Liam, Lucy, Martin, Matt, Phil, Sarah, Tim, Will and of course my fellow ‘Cabbages’: Becca, Becky, Cat, Cata, Danni P, Freydís, Jo, José, Kelly, Mikey, Siân, Tom, Vero and Wayne. Thank you all for the helpful discussions, uncontrollable laughter, badminton, volleyball and general distraction. During this PhD, I’ve spent a good deal of time at the NERC facilities at Sheffield University. My time there was always a pleasure (even when the lab work wasn’t!) and I thank all the visiting researchers and staff who made my stays both productive and enjoyable. Particular thanks go to Andy, Gav and Debs for sharing lab woes, tea and friendship. A very special thanks to Maria- Elena, I owe you big time my friend. Thank you to everyone in the Republic of Seychelles that made my fieldwork in paradise something to treasure. Particular thanks to Nature Seychelles and the staff of Cousin Island: April, Aurélien, Dan, Dorothy, Ian, Jessica, Liz, Mary, Nirmal and Riaz and to the proprietors and staff of Aride, Cousine and Frégate – particularly Greg, Kevin, Licia, San-Marie and Tatiana for making it feel like home from home…well ok, maybe home but with a ‘little extra’ sunshine! Mum, Dad, Dan, Ems and the rest of the clan: you are nothing short of inspirational and I thank each of you for your encouragement, love and belief in me. I will repay you for forgetting where the phone was when away, but always seeming to remember where the fridge and pantry were when I came home! Thanks also to my in-laws Andrew, Joy, Ethan, Anna, Paul, Jo, John, Chris and Steve. Thonoir, Paul R, Emma T – thanks for your continued support. Laura, I cannot thank you enough for the endless love, support, encouragement, comfort and cake you have given, and continue to give to me. You made my whole PhD experience that much richer and more enjoyable (and even courageously married me half way through it all!). I’m truly in your debt. Tea, anyone…? iv Contents Page Abstract iii Acknowledgements iv Chapter contributions vi Chapter 1 1 General Introduction Chapter 2 33 Museum DNA reveals the demographic history of the endangered Seychelles warbler Chapter 3 61 The impact of translocation on neutral and functional genetic diversity within and amongst populations of the Seychelles warbler Chapter 4 91 Translocation of the Seychelles warbler to Frégate Island, Seychelles Chapter 5 103 Experimental investigation of MHC-dependent social mate choice in Seychelles warblers Chapter 6 124 Investigating MHC-dependent survival and reproduction in the Seychelles warbler Chapter 7 154 General discussion v Author Contributions At the time of final submission, three of the five data chapters presented in this thesis are published and one is in review. I am lead or joint-lead author on all manuscripts and I have made by far the largest contribution to the work presented in this thesis. Below, I provide a citation for each data chapter, highlight authorship and specify my contributions. Chapter 2: Spurgin LG*, Wright DJ*, Van der Velde M, Collar NJ, Komdeur J, Burke T & Richardson DS (2014) Evolutionary Applications doi: 10.1111/eva.12191. - DJW role in locating and sampling museum specimens, lab work and drafting manuscript (40%). * joint primary authorship Chapter 3: Wright DJ, Spurgin LG, Collar, NJ, Komdeur J, Burke T & Richardson DS (2014) Molecular Ecology 23 , 2165-2177. - DJW role in designing the study, fieldwork and translocation (Frégate), lab work, lead data analyses and drafting manuscript (75%) Chapter 4: Wright DJ, Shah NJ & Richardson DS (2014) Conservation Evidence 11 , 20-24. - DJW role in translocation and drafting manuscript (70%) Chapter 5: Wright DJ, Mannarelli ME, Komdeur J, Burke T & Richardson DS (in review: Behavioral Ecology ) - DJW role in fieldwork, lab work, lead data analyses and drafting manuscript (70%) Chapter 6: Wright DJ, Spurgin LG, Dugdale HL, Komdeur J, Burke T & Richardson DS (in prep.) - DJW role in lab work, lead data analyses and drafting manuscript (65%) vi Chapter 1 General introduction © David Wright Cousin Island, with Praslin Island in the background Chapter 1: General introduction 1.1 Challenges in evolutionary and conservation genetics “…reinforcing the grounds for nature conservation with an evolutionary perspective may help to give conservation a permanence which a utilitarian, and even an ecological grounding, fail to provide in men’s minds.” Otto Frankel, 1974 Evolutionary and conservation genetics are both concerned with the ability of populations to evolve in response to environmental change (Reed & Frankham 2001). A central principle of evolutionary biology is that evolutionary change depends on heritable variation. Consequently, the ability of species to evolve is primarily determined by adaptive, or functional, genetic variation (Frankham 2010). Understanding the amount and persistence of this variation
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