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Detecting Inbreeding Depression in a Severely Bottlenecked, Recovering Species: the Little Spotted Kiwi (Apteryx Owenii)

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Detecting inbreeding depression in a severely bottlenecked, recovering species: the little spotted kiwi (Apteryx owenii) Helen R. Taylor A thesis submitted to Victoria University of Wellington in fulfilment of the requirement for the degree of Doctor of Philosophy in Ecology and Biodiversity Victoria University of Wellington Te Whare Wānanga o te Ūpoko o te Ika a Māui 2014 This thesis was conducted under the supervision of Dr. Kristina Ramstad1, AProf. Nicola Nelson1, Prof. Fred Allendorf2 & Dr. Hugh Robertson3 1Allan Wilson Centre, Victoria University of Wellington, Wellington, New Zealand 2Montana Conservation Genetics Lab, University of Montana, Missoula, USA 3New Zealand Department of Conservation, Wellington, New Zealand All images featured in this thesis were created or taken by the author unless otherwise stated. Abstract Population bottlenecks reduce genetic variation and population size. Small populations are at greater risk of inbreeding, which further erodes genetic diversity and can lead to inbreeding depression. Inbreeding depression is known to increase extinction risk. Thus, detecting inbreeding depression is important for population viability assessment and conservation management. However, identifying inbreeding depression in wild populations is challenging due to the difficulty of obtaining long-term measures of fitness and error-free measures of individual inbreeding coefficients. I investigated inbreeding depression and our power to detect it in species that have very low genetic variation, using little spotted kiwi (Apteryx owenii) (LSK) as a case study. This endemic New Zealand ratite experienced a bottleneck of, at most, five individuals ~100 years ago and has since been subjected to secondary bottlenecks as a result of introductions to new predator-free locations. There is no behavioural pedigree data available for any LSK population and the status of the species is monitored almost exclusively via population growth. I conducted two seasons of field work to determine hatching success in the two LSK populations with the highest and lowest numbers of founders; Zealandia Sanctuary (40 founders) and Long Island (two founders). I also used simulation-based modelling to assess the feasibility of reconstructing pedigrees based on individual genotypes from LSK populations to calculate pedigree inbreeding coefficients. Finally, I used microsatellite genotypes to measure the genetic erosion in successive filial groupings of Long Island and Zealandia LSK as a result of their respective bottlenecks, and tested for inbreeding depression on Long Island. Hatching success was significantly lower on Long Island than in Zealandia in both years of the study despite significantly higher reproductive effort on Long Island. Although this was suggestive of inbreeding depression on Long Island, simulation results showed that constructing a pedigree for any LSK population based on the genetic markers and samples currently available would lead to inaccurate pedigrees i and invalid estimates of individual inbreeding coefficients. Thus, an alternative method of detecting inbreeding and inbreeding depression was required. Microsatellite data showed continued loss of heterozygosity in both populations, but loss of allelic diversity on Long Island only. Individual genotypes indicated that the majority (74%) of the adult Long Island population is comprised of the founding pair (F) and their direct offspring (F1) rather than birds from subsequent generations (F2+). This is not what would be expected if survival was equal between these two filial classes. I suggest that the high levels of inbreeding (≥0.25) in F2+ birds is impacting on their survival, creating a demographic skew in the population and resulting in lower hatching success on average on Long Island when compared to the relatively outbred Zealandia birds. This inbreeding depression appears to have been masked, thus far, by positive population growth on Long Island resulting from the long life span of LSK (27-83 years) and continued reproductive success of the founding pair. Thus, it is likely that the Long Island population will go into decline when the founding pair cease to reproduce. This study highlights the challenges of measuring inbreeding depression in species with very low genetic variation and the importance of assessing the statistical power and reliability of the genetic tools available for those species. It also demonstrates that basic genetic techniques can offer valuable insight when more advanced tools prove error-prone. Monitoring vital rates such as hatching success in conjunction with genetic data is important for assessing the success of conservation translocations and detecting potentially cryptic genetic threats such as inbreeding depression. My results suggest that LSK are being affected by inbreeding depression and that careful genetic management will be required to ensure the long-term viability of this species. ii Acknowledgements I am grateful to my supervisors, Kristina Ramstad, Nicky Nelson and Fred Allendorf. A PhD is, more than anything, a learning degree and I have learned a huge amount from working with these three people. They have been supportive, informative and challenging when necessary and I have benefitted enormously from their combined knowledge and experience. My advisor at the Department of Conservation, Hugh Robertson and his colleague Rogan Colbourne were generous enough to share their extensive knowledge of little spotted kiwi with me. As an English researcher arriving in New Zealand with very little knowledge of kiwi, I was lucky to have access to the unparalleled experience that Hugh and Rogan share between them. They were also kind enough to introduce me to their kiwi tracking dogs, Cara, Jade and Abbie, who were a great help during my field work. The Zealandia kiwi “stalkers”: Judy Briggs, Heather Constable, Erin Daldry, Chris Gee, Anna Grant, Karen Koopu, Linton Miller and Bronwyn Shepherd are an amazing group of people who all went the extra mile for this project and who never ceased to amaze me with their good humour and enthusiam. Tristam Price was a great help in maintaining and monitoring the camera traps used in Zealandia. I am also very grateful to the 40+ people who turned out to help with the 2011/12 little spotted kiwi radio tag change effort A variety of volunteers were brave enough to accompany me to my second field site, Long Island. I am very grateful to Rachael Abbott, Helen Armstong, Sacha Astill, Emma Bean, Judy Briggs, Jo Carpenter, Rogan Colbourne, Heather Constable, Andrew Digby, Mark Dodds, Luke Dunning, Fred Gaudin, Katy Gibbs, Elizabeth Heeg, Duncan Kay, Sue Keall, Isla McGregor, Steph Price, Riki Mules, Claire Raisin, Kristina Ramstad, Hugh Robertson, Bronwyn Shepherd and Rachel Wilcox for making the trip and bashing through numerous flax bushes on numerous cliff edges in search of errant birds and their nests. iii My field work on Long Island was facilitated in no small way by the team at Cougar Line water taxis in Picton. Cougar Line’s owners, Jill and Mark Evans, not only provided me with transport to and from Long Island, but also allowed me to train their boat skippers to collect radio telemetry data from the site by boat. I am particularly grateful to boat skipper Fred Gaudin, and Bill Shirley for stepping in to help with data collection when Fred was busy with his real job. Interislander ferries kindly provided free return transport from Wellington to Picton for each Long Island field trip, which was a major cost saving. During the course of my studies, I was lucky enough to collaborate with one of Fred’s other PhD students over in the States, Marty Kardos. Marty has been a great sounding board for numerous ideas, was kind enough to lend me his R-scripts for my pedigree simulation work, and allowed me early access to some of his own manuscripts. He is a brilliant geneticist and patient teacher. James Fraser and Tash Coad plus their dogs Percy and Breeze worked tirelessly to help me find more kiwi in a shorter space of time than most people would consider reasonable. Raewyn Empsom at Zealandia facilitated my access to the site and offered advice based on her wealth of experience in conservation. The Department of Conservation staff in Picton, particularly Bill Cash, ensured my Long Island trips went off without a hitch. Kevin Buckley helped me get my head around how to use the VUW Condor computing platform. Claire Travers at Kiwi Encounter guided me through the grizzly process of kiwi egg autopsies. John Wilks schooled me in the finer points of Chick TimerTM software and was always on hand with detailed answers to my numerous questions. Chris Milne at Sirtrack made sure I had the best radio tags available for little spotted kiwi. Andrew Digby shared a large amount of little spotted kiwi (and later statistical) knowledge with me throughout the course of my study and I am indebted to his generosity. Anna Carter has been incredibly patient with me in sharing her impressive knowledge of R. My study was funded by the Allan Wilson Centre, Victoria University of Wellington, the Centre for Biodiversity and Restoration Ecology, the New Zealand Ministry for iv Business, Innovation and Employment and Kaitiaki o Kapiti Trust. I am also grateful to Waiorua Bay Trust, Kaitiaki o Kapiti Trust, Te Atiawa Manawhenua ki te Tau Ihu Trust and Port Nicholson Block Settlement Trust for their co-operation with this project. I consider myself lucky to have been a part of the Allan Wilson Centre and to have had the chance to meet and discuss my work with all the talented people in that group. Doing a PhD thousands of miles from home is (I see now) an interesting choice. Fortunately, I have an excellent network of friends in Wellington who have become part of my extended family, in particular Heather Constable, Elizabeth Heeg, Rachael Abbott, Janey Walker and Lida Ayoubi, who have all been very supportive and, more importantly, fun people to be around. Judy Briggs and Karen Koopu have been the best NZ aunties I could have wished for and have given me so may opportunities to experience the amazing landscape of Aotearoa.
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