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The Evolutionary Genetics of Meerkats (Suricata Suricatta)

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The Evolutionary Genetics of Meerkats (Suricata Suricatta) The evolutionary genetics of meerkats (Suricata suricatta) Johanna F. Nielsen Submitted for the degree of Doctor of Philosophy The University of Edinburgh 2012 Declaration I declare that the work described in this thesis has been carried out by myself unless otherwise acknowledged. It is entirely of my own composition, the main text and bibliography do not exceed 70,000 words, and it has not, in whole or part, been submitted for any other degree. Johanna F. Nielsen December 2012 i ii Dedication Till Aaron Ibbotson den mest förstående och tålmodiga människa jag känner med all min kärlek iii iv Abstract Cooperative species have long been the focus of much research due to the ‘special difficulty’ cooperation poses to the theory of evolution via natural selection. Despite this long history of scientific interest we actually know relatively little about the evolutionary genetics of cooperative mammalian species, especially in the wild. In this study I use long-term data from the Kalahari Meerkat Project to investigate some aspects of the evolutionary genetics of meerkats (Suricata suricatta). First, I reconstructed a genetically-validated pedigree of the Kalahari meerkat population. 1,494 meerkats (83% of the total known population) were genotyped at a panel of 18 highly variable microsatellite markers. This genetic data, in combination with phenotypic information and two different programs, COLONY2 and MASTERBAYES, was used to infer familial relationships. The resulting pedigree spanned seven generations and included 1,614 individuals of which 1,076 had both parents known. I conclude by discussing the particular merits of using COLONY2 to infer familial relationships for social animals such as meerkats. Second, I investigated the extent of inbreeding and inbreeding depression in early life traits in the Kalahari meerkat population. In the pedigree, 44% of individuals have non-zero (F>0) inbreeding coefficients. Although I found more inbreeding in meerkats than initially expected, there were few cases of inbreeding between very close relatives. Nonetheless, even low to moderate inbreeding appeared to result in inbreeding depression for pup mass at emergence, hind-foot length, growth until independence, and juvenile survival. I also found some tentative evidence for a positive effect of the social environment in ameliorating the effects of inbreeding depression. Third, I conducted a quantitative genetic analysis on mass, skull length, skull width, forearm length, and hind-foot length in up to five key meerkat life stage periods, while accounting for a number of fixed effects, including inbreeding coefficient. By attempting to apportion variance in these traits to a variety of sources I found that birth litter identity often explained much of the variance in morphological traits, although the magnitude of this effect appeared to decline with age. Furthermore, when birth litter was removed from models, the amount of variance explained by additive genetic effects tended to increase. Finally, I conducted a quantitative genetic analysis on two measures of cooperative care and on adult mass. Fixed effects, including inbreeding and relatedness coefficients, were also examined, which revealed that inbred individuals contribute more to pup-feeding, and that helper-recipient relatedness was negatively associated with baby-sitting. I found low heritable variation for baby-sitting (h2 = 0.10) and pup-feeding (h2 = 0.08), and higher heritable variation for adult body mass (h2 = 0.19). I also estimated the magnitude of non-genetic sources of variation in these traits and provide evidence for positive genetic correlations between baby-sitting and pup-feeding, and baby-sitting and adult mass. v vi Acknowledgements First and foremost, a huge thank-you to my supervisory team, Josephine Pemberton, Loeske Kruuk and Jinliang Wang. Josephine has been an incredibly generous, encouraging and inspiring principal supervisor and I am enormously grateful for every bit of her time, advice and support. Her genuine enthusiasm and dedication to all aspects of academic research has been truly infectious. I am also deeply indebted to Loeske for her constant encouragement, flexibility, moral boosts and willingness to find time to patiently clarify complex issues to me. Similarly, Jingliang Wang has the amazing ability to explain complicated theory and methods in a simple way and was always extremely welcoming, supportive and generous with his time when I was in London. In addition to my official supervisors, this PhD research would of course not have been possible without Tim Clutton-Brock, who established and continues to maintain the field site, together with Marta Manser (University of Zurich). Furthermore, Tim always made me feel warmly welcomed at Cambridge and his advice and feedback have been much appreciated. The combination of these supervisors meant I was lucky enough to get to work with a variety of people at several different institutions. Firstly, in Edinburgh I have endless amounts of appreciation and admiration for Will Goodall-Copestake who ensured I enjoyed my time in the lab by developing and optimizing a marvelous suite of meerkat microsatellite makers. Sheena Morrissey was a wonderfully conscientious lab assistant who greatly eased my workload by helping me churn through the genotyping as fast as possible. Together with Liz Heap and Claire Webster, Sheena also provided invaluable companionship and good humor when I was confined to the lab. I would also like to thank the GenePool for processing my multitude of genotyping samples so swiftly. Out of the lab, I have been much assisted by Ian Stevenson and his Access database wizardry, whose powers I continue to remain in awe of. I have also benefited enormously from the help of Jarrod Hadfield who has been incredibly patient with my seemingly endless stream of MASTERBAYES and general statistics questions. Similarly, Craig Walling and Michael Morrissey have also graciously endured a number of my statistical queries: I am particularly grateful that Craig ‘paved the way’ for me so brilliantly with his work on the red deer pedigree and subsequent inbreeding analyses, and for Michael’s thorough understanding of MCMCGLMM. I had the great pleasure of first meeting Matt Bell in the field, several times in Cambridge and then welcoming him as a member of the Wild Evolution Group (WEG) in Edinburgh. It was brilliant to have such a knowledgeable meerkatologist up North and I am grateful for all the advice and comments he gave me. In general I feel very fortunate to have been a member of WEG and I’d like to thank all members of the group for making my time in Edinburgh so memorable. Finally, I’d like to thank my fellow PhD cohort members, Rebekah Watt, Lynne Harris, Matty Hartfield, Fiona Lethbridge, Marisa Magennis and Harriet Stone, and everyone else who made sure my time at the Institute of Evolutionary Biology (IEB) so enjoyable. vii viii The supervision of Jinliang and a CASE partnership enabled me to maintain links with the Institute of Zoology (IoZ) in London, which has been beneficial to me in many ways and I would therefore like to thank the Zoological Society of London for providing me with this opportunity. I have relished the time I’ve spent back at the IoZ and would particularly like to thank Bill Jordan, who started as my boss but quickly grew to be a friend and who was always wonderfully supportive and kind - he is missed terribly. It was always a treat for me to spend time with fellow meerkatologists at the Large Animal Research Group (LARG) in Cambridge and I appreciate the effort everyone made to make me feel welcome there. During the course of this PhD I have had the great fortune of collaborating with a number of LARGites: Andrew Bateman assisted me with statistical analyses, and, Sinead English provided me with her extremely valuable cooperative care and morphological data in an enthusiastic and wonderfully agreeable way. I’d also like to thank Stu Sharp for fielding a variety of my questions, and all other LARG members for their comments and hospitality in Cambridge. I owe a huge debt of gratitude to the countless number of past and present project managers, field staff, volunteers, PhD and MSc students, and post-doctoral researchers at the Kalahari Meerkat Project in South Africa. It was they who collected all the data and samples and thus ultimately made this research possible. I am extremely grateful and admiring of all their hard work. I would especially like to thank Tom Flower, Rob Sutcliffe, Megan Price, Jamie Samson and Nathan Thavarajah who have al been project mangers, some of who welcomed me so wonderfully at the study site when I visited. Finally. I would like to thank my friends and family for all their continued support and encouragement over the years, but especially Julia Latham, Jonathan Peek, Karin Nielsen and Peter Hunter for their proof reading, IT help and additional understanding. Most importantly, no words can thank Aaron Ibbotson enough for his endless levels of support and patience and for never uttering anything other than words of encouragement. This research was supported financially by a Natural Environment Research Council doctoral grant, the Universities of Edinburgh and Cambridge and a CASE partnership with the Zoological Society of London, for which I am most grateful. ix x Table of contents Declaration i Dedication iii Abstract v Acknowledgements vii Table of contents xi Paper arising from this thesis xvii List of appendices xix List of tables xxi List
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