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The Role of Inbreeding in the Reproductive Fitness of Kakapo (Strigops Habroptilus)

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The Role of Inbreeding in the Reproductive Fitness of Kakapo (Strigops Habroptilus) The role of inbreeding in the reproductive fitness of kakapo (Strigops habroptilus) A thesis submitted for the degree of Masters of Wildlife Management at the University of Otago, Dunedin, New Zealand Kaitlyn White June 2012 i Abstract As populations decline, inbreeding becomes increasingly unavoidable. Increased genome- wide homozygosity for inbred individuals can result in reduced survival and reproductive fitness (i.e. inbreeding depression), via the expression of deleterious recessive alleles and reduced heterozygosity at over-dominant loci. The tendency for deleterious recessive alleles to drift to high frequencies in small populations means that inbreeding depression can be particularly severe for threatened populations. Therefore, the genetic consequences of small and isolated populations are becoming of increasing concern to conservation biologists. The kakapo (Strigops habroptilus) is a critically endangered, flightless, nocturnal parrot that now survives only on predator-free island sanctuaries in New Zealand. The recent population bottleneck of 51 individuals, lek mating system and insular origin of all but one of the surviving kakapo, render them particularly susceptible to inbreeding depression. Low productivity of kakapo has been reported and potentially attributed to, an aging population, diet and inbreeding. For this reason, the present study investigated the relationship between inbreeding and reproductive fitness in kakapo. The preferred method of assessing inbreeding is to use multi-generational pedigree information. However, this is currently unavailable for kakapo, therefore molecular estimates of relatedness were used as a surrogate for pedigree-derived inbreeding coefficients. Internal relatedness and pairwise relatedness were calculated using 25 polymorphic microsatellite loci. The link between relatedness estimates and variation in early life history traits was investigated using heterozygosity-fitness correlations. This was achieved through the use of generalised linear mixed modelling, with an information-theoretic approach and model averaging where necessary. The reproductive traits investigated were female fecundity (clutch size), egg fertility (probability of an egg being fertilised by an individual male), hatching success of fertile eggs (proportion of fertile eggs that a female hatches) and sperm quality (concentration, motility and morphology). Neither variation in female fecundity nor egg fertility could be attributed to homozygosity with any confidence. Hatching success was determined to be strongly reduced for the more homozygous females and the more homozygous males were determined to have significantly higher proportions of abnormal sperm. Therefore, the present study demonstrated that inbreeding depression is a contributing factor towards reduced reproductive success in kakapo. These findings are consistent with known detrimental effects of inbreeding, in particular for New Zealand endemic species that have experienced severe ii population bottlenecks. To minimise these effects, and hence reduce potential impacts on population growth and species recovery, kakapo managers should aim to prevent further erosion of genetic diversity and to breed from the descendants of the genetically-distinct Fiordland male Richard Henry. The present study highlights the importance of considering the genetic components of populations in any conservation management program. iii Acknowledgements This study was made possible by the generous support and assistance from a number of people. Endless thanks to the best supervisors anyone could ask for, Dr Bruce Robertson and Associate Professor Ian Jamieson. Your guidance, patience and editorial comments along the way were invaluable in helping me produce this work. Thanks to Bruce for giving me access to the genetic data for kakapo (the “Matrix”) and to those who have helped him put it together over the years (Fiona Robertson and Karin Ludwig). Thanks to the Department of Conservation and the kakapo recovery team, in particular Daryl Eason, for providing me with all the monitoring data. You guys made this research possible by your tireless commitment to the conservation of kakapo. Thanks also for allowing me time on Whenua hou to experience the magic of being around kakapo and to appreciate all the hard work that goes into managing these birds. Great appreciation goes to the Threatened Bird Research Group who provided helpful discussions and ideas along the way, especially Dr Catherine Grueber and Sheena Townsend for assistance and clarification through my time carrying out the statistical analyses. Thanks to my helpful proof readers: Anne, Hayden and Martin. Thanks also to the friendly Zoology Department at the University of Otago; the regular tea, coffee, scones and happy hours were a huge help. And to my office mates, you guys were the best, thanks for all the good times and enjoyable work environment! Many thanks to all my family, you have all been there for me and have supported me all the way, you really made this possible and I will be forever thankful. Thanks mum and dad for always believing in me and helping me achieve everything I stubbornly set my mind to. Special mention to my flatmates Carmen and Richie for really being there when I needed you and getting me through to the end! This work was generously supported by the University of Otago Postgraduate Masters Scholarship for Students of Maori Descent, the Ngai Tahu Tertiary Education Fund and the Department of Conservation’s Kakapo Recovery Group (research contracts to Bruce Robertson). iv Table of Contents Title ......................................................................................................................................... i Abstract .................................................................................................................................. ii Acknowledgements ............................................................................................................... iv Table of Contents ................................................................................................................... v List of Tables ...................................................................................................................... viii List of Figures ....................................................................................................................... ix List of Appendices ................................................................................................................ ix Chapter 1: General Introduction ........................................................................................... 1 1.1 General background ......................................................................................................... 2 1.2 Inbreeding depression ...................................................................................................... 2 1.2.1 Definition ................................................................................................................... 2 1.2.2 Fitness impacts and magnitude of effects .................................................................. 3 1.3 Estimating relatedness ...................................................................................................... 5 1.3.1 Pedigree estimates ..................................................................................................... 5 1.3.2 Molecular estimates ................................................................................................... 6 1.4 Heterozygosity-fitness correlations .................................................................................. 7 1.5 Kakapo ecology and conservation status ......................................................................... 8 1.5.1 Kakapo monitoring and management ........................................................................ 9 1.5.2 Genetic diversity of kakapo ..................................................................................... 10 1.6 Research aims ................................................................................................................. 11 1.7 Thesis structure .............................................................................................................. 12 Chapter 2: The Effects of Inbreeding on Kakapo Fecundity, Egg Fertility and Hatchability ............................................................................................................................ 14 2.1 Introduction .................................................................................................................... 15 2.1.1 Study aims ............................................................................................................... 16 v 2.2 Materials and methods ................................................................................................... 17 2.2.1 Monitoring data ....................................................................................................... 17 2.2.2 Molecular methods .................................................................................................. 18 2.2.3 Estimating relatedness ............................................................................................. 18 2.2.4 Model fitting ............................................................................................................ 20 2.3 Results ...........................................................................................................................
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