Inbreeding and Fitness in Wild Ungulates
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Inbreeding and fitness in wild ungulates Tristan C. Marshall A thesis submitted to The University of Edinburgh in application for the degree of Doctor of Philosophy June 1998 "Nothing happens in contradiction to nature; only in contradiction to what we know of it. Dana Scully, The X Files 1997 Preface This thesis has been composed by me, is the result of my own research and contains no work done in collaboration except where stated otherwise. The text does not exceed 100,000 words. No part of this thesis has been submitted to any other university in application for a higher degree. 111 Summary Inbreeding and the effects of inbreeding on the fitness of individuals have been studied extensively for over a century. Surprisingly, there have been few studies of the fitness consequences of inbreeding in wild animal populations. In this thesis I examine inbreeding and its fitness consequences in two species of wild ungulates, red deer (Cervus elaphus) and Arabian oryx (Oryx leucoryx). The long term study of red deer on the Isle of Rum has included profiling of individuals at polymorphic protein and microsatellite loci. I developed a likelihood- based method for large-scale paternity inference and implemented it via the computer program CERVUS. The system allowed genetic inference of paternity with 80% confidence for 536 red deer calves. I used these data to construct pedigrees and found that 11% of calves were the offspring of matings between paternal half sibs; however most inbreeding coefficients were zero. Microsatellite-based measures of inbreeding and outbreeding, individual heterozygosity and mean d2, were calculated using data from nine microsatellite loci. Among stags born 1982-1986, neither individual heterozygosity nor mean d2 influenced survival to reproductive age, while mean d2 but not individual heterozygosity positively influenced stag lifetime mating success (LMS) among males which reproduced. Among hinds born 1982-1986, individual heterozygosity but not mean d2 positively influenced survival to reproductive age and age at first breeding among hinds which reproduced, while mean d2 (in an interaction with year of birth) but not individual heterozygosity influenced hind LMS. Arabian oryx went extinct in the wild in 1972 and were reintroduced to Oman and Saudi Arabia after several generations of breeding in captivity. 343 Arabian oryx representing several major populations were typed at six microsatellite loci. Average heterozygosity and differentiation between groups were low. In reintroduced Arabian oryx in Oman no relationship was found between inbreeding coefficient and juvenile survival. However individual heterozygosity was positively related to juvenile survival while mean d2 was negatively related to juvenile survival, implying simultaneous inbreeding and outbreeding depression. Genetic, environmental and anthropogenic factors all influence the survival of reintroduced Arabian oryx, but despite the joint influence of these factors, the Omani population is growing rapidly. iv Acknowledgements The work presented in this thesis would have been impossible without the help of many people. The Arabian oryx project in Oman was initiated by Ralph Daly with funding from Sultan Qaboos bin Said, and the project was run in the early years by Mark Stanley Price. I particularly thank Andrew Spalton for providing hospitality, samples and unpublished data from his thesis, and thanks are also due to Ralph and Elizabeth Daly, Robert and Anna Lewellyn-Smith and Stephen Brent for hospitality in Oman. Additional samples were provided by Mark Lawrence, Oliver Ryder and Helen Stanley, with grateful thanks to Paul Sunnucks for assembling such a large collection of samples and helping me to identify their origin, to Sarah Christie for supplying studbook data, to Georgina Mace for supplying the program FASTINB needed to analyse that data and to Rob Hammond for his gazelle primers. I also thank Jelle Boef and Khaldoon Kiwan (RSCN, Amman) for their hospitality in Jordan. Finally (in this first bit) Stdphane Ostrowski (NWRC Tall) and Jaime Samour (Fahad bin Sultan Falcon Centre, Riyadh) gave invaluable criticism on and additional information for Chapter 7, and I particularly thank Stéphane and all at NWRC for visa acquisition, their generous hospitality and in particular their surprisingly palatable brand of accidentally fermented grape juice. For the red deer project on Rum, Tim Clutton-Brock, Steve Albon and especially Fiona Guinness contributed a huge amount of observational data collected between 1971 and 1996, assisted latterly by Colleen Covey, Angela Alexander and Ailsa Curnow as well as countless volunteers. I acknowledge the support of Scottish Natural Heritage, owners of Rum, and BBSRC and NERC for long term project funding, and thank Fiona Guinness and Ailsa Curnow for hospitality and entertainment on and off Rum. Josephine Pemberton collected most of the samples on Rum, carried out allozyme typing and cloned microsatellites, while Jon Slate performed the Herculean task of typing more than 1,000 deer at ten microsatellite loci. I must also thank Mark Beaumont for coming up with an awesomely good idea which I never would have thought of and Tim Coulson for putting it into practice and also patiently explaining General Linear Models to me and providing most excellent hospitality. v Thanks to Simon Goodman, David Bancroft and Bill Amos for program code which was incorporated into the CERVUS program, Nick Barton for another good idea which I wouldn't have thought of and Loeske Kruuk for her invaluable help with the use of likelihoods and with the deer work generally. Penny Allen, Elena Valsecchi, Judith Smith, Dave Coltman and Ashleigh Griffin offered up their data sets for butchery by early versions of CERVUS and gave me many insights into ways I could improve the program. I feel that Graeme Swanson, Steve Paterson, Ian Stevenson and Jill Pilkington should also appear somewhere in these acknowledgements and this seems like as good a place as any. I would also like to thank the BBSRC for financial support, the DSS for liberal interpretation of the phrase "actively seeking work", my family for their continuous moral support and generous credit terms, and John Deag and Vernon French for offering me a ladder to liquidity as well as the opportunity to learn some statistics at the expense of the 1997-1998 Zoology Honours class. The last-but-not-least final round of thanks go to all past and present members of the Molecular Ecology lab in Cambridge and Edinburgh for tolerating my endless questions and Fresh Air FM, to my flatmates Katrina Lythgoe and Amanda Voase for putting up with my nocturnal comings and goings over the last few months and most importantly to the head canary keeper, Josephine Pemberton, for encouraging and guiding me through this PhD and for fantastic criticism of the thesis itself, without which it would have been unimaginably worse than it is now. I am sure I am guilty of many errors and omissions both in these acknowledgements and in the thesis as a whole. For these and everything else I apologise. Right, I'm off to the pub. vi Table of contents Preface......................................................................................................................... iii Summaiy....................................................................................................................... i v Acknowledgements........................................................................................................ v Tableof contents ......................................................................................................... Vii 1 Introduction .................................................................................................... 1 1 .1 In the beginning ... .................................................................................................... i 1.2 Theory and techniques.............................................................................................2 1.3 Empirical data........................................................................................................10 1.4 Outline of the thesis...............................................................................................22 2 Red deer on Rum.........................................................................................23 2.1 Introduction............................................................................................................23 2.2 History of the population.......................................................................................25 2.3 Ecological and behavioural work...........................................................................28 2.4 Genetic work..........................................................................................................30 2.5 Inbreeding and fitness in Rum red deer.................................................................36 3 Likelihood-based paternity inference using microsatellites....................38 3.1 Introduction............................................................................................................38 3.2 Methods .................................................................................................................41 3.3 Results....................................................................................................................49 3.4 Discussion..............................................................................................................58