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Translocations and the 'Genetic Rescue' of Bottlenecked Populations

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Translocations and the 'Genetic Rescue' of Bottlenecked Populations Translocations and the ‘genetic rescue’ of bottlenecked populations ATHESIS SUBMITTED IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY IN WILDLIFE CONSERVATION AT THE UNIVERSITY OF CANTERBURY SOL HEBER SEPTEMBER 2012 Abstract Many species around the world have passed through severe population bottlenecks due to an- thropogenic influences such as habitat loss or fragmentation, the introduction of exotic predators, pollution and excessive hunting. Severe bottlenecks are expected to lead to increased inbreed- ing depression and the loss of genetic diversity, and hence reduce the long-term viability of post- bottlenecked populations. The objective of this thesis was to examine both the consequences of severe bottlenecks and the use of translocations to ameliorate the effects of inbreeding due to bot- tlenecks. Given the predicted increase in probability of inbreeding in smaller populations, one would expect inbreeding depression to increase as the size of a population bottleneck decreases. Deter- mining the generality of such a relationship is critical to conservation efforts aimed at minimising inbreeding depression among threatened species. I therefore investigated the relationship between bottleneck size and population viability using hatching failure as a fitness measure in a sample of threatened bird species worldwide. Bottleneck size had a significant negative effect on hatch- ing failure, and this relationship held when controlling for confounding effects of phylogeny, body size, clutch size, time since bottleneck, and latitude. All species passing through bottlenecks of ∼100–150 individuals exhibited increased hatching failure. My results confirm that the negative consequences of bottlenecks on hatching success are widespread, and highlight the need for conser- vation managers to prevent severe bottlenecks. In many endangered species, preventing bottlenecks is no longer an option as populations have already declined to a level where urgent action is required to mitigate the negative effects of in- breeding and ensure their long-term viability. In the past, two approaches have been used with some success: (1) the introduction of outbred individuals into inbred populations, and (2) the aug- mentation of inbred populations through the release of captive-reared individuals. However, both approaches have limitations. For example, in many threatened species, there are no outbred pop- ulations left to use as a source for introducing new individuals into inbred populations. Similarly, captive populations may not be available, and if they are, individuals may also be inbred and adapted to captivity, and perhaps less likely to survive in free-living conditions. I therefore experimentally 2 tested whether reciprocal translocations between different inbred populations could be an alterna- tive technique to mitigate the negative effects of inbreeding and restore levels of genetic variation once a species or population has passed through a bottleneck. First, I conducted a laboratory experiment using inbred lines of the fruit fly Drosophila mela- nogaster. I used founding populations of just one male and one female to create replicate inbred lines in two different strains of fruit flies. After two generations of inbreeding, I found that cross- ing individuals between the two bottlenecked strains reversed the effects of inbreeding and led to increases in overall breeding success and survival that persisted into the second generation of hy- brid offspring. In contrast, crosses within each strain (but between different replicate lines) resulted in only slight improvements in some fitness components, and this positive trend was reversed in the second generation. The results of this experiment suggest that inbred populations can be used as donors to reduce the effects of severe population bottlenecks and ‘rescue’ an endangered species from inbreeding depression but that the effect is strongest if there are some initial genetic differences between donor populations. To confirm whether ‘genetic rescue’ through the use of inbred populations can be used in a free-living animal, I repeated the above experiment in a natural setting by conducting reciprocal translocations between two severely bottlenecked and isolated South Island robin Petroica australis populations. Both populations had been founded by just five birds each and showed signs of in- breeding depression. I found significant increases in mean levels of heterozygosity in the hybrid offspring (crosses between the two populations) compared to inbred control offspring. Similarly, allelic richness increased significantly in both populations within the first year after the transloca- tion. The significant increase in genetic diversity was accompanied by increases in overall levels of fitness. Hybrid birds experienced increased levels of both survival and recruitment into the breeding population, and sperm quality improved significantly in hybrid males compared with inbred males. Finally, I found a significant increase in one aspect of cell-mediated immunity in hybrid individuals. The results of the field study using robins confirm the pattern found in the laboratory with fruit flies and highlight that inbred populations should not be discounted as potential donors for genetic rescue when outbred populations are unavailable. In conclusion, the finding that the negative effects of inbreeding increase with the severity of the population bottleneck experienced provides added impetus for conservation biologists to ensure endangered species do not pass through severe bottlenecks. For species or populations that are 3 already affected by inbreeding depression and have no outbred populations left to act as a source for the introduction of new genetic stock, the results of both the laboratory and the wild experiment confirm the potential value of translocations between different inbred populations of endangered species as a tool to mitigate the negative effects of inbreeding. In order to ensure the long-term viability of any threatened species or population, however, it is essential to realise that genetic interventions in form of reciprocal translocations need to be complemented with other management strategies aimed at the restoration or conservation of suitable habitat. Table of Contents Abstract . 1 Table of Contents . 5 List of Figures . 11 List of Tables . 13 Acknowledgements . 15 1 General Introduction 19 Outline of the thesis . 26 References . 28 2 Population bottlenecks and increased hatching failure in endangered birds 39 2.1 Introduction . 40 2.2 Material and methods . 41 2.2.1 Data collection . 41 2.2.2 Data analyses . 42 2.3 Results . 43 2.4 Discussion . 44 References . 51 3 A test of the ‘genetic rescue’ technique using bottlenecked donor populations of Drosophila melanogaster 59 5 6 3.1 Introduction . 60 3.2 Material and methods . 61 3.2.1 Inbreeding method . 61 3.2.2 Crossing experiments . 62 3.2.3 Breeding success . 64 3.2.4 Survival . 64 3.2.5 Data analyses . 64 3.3 Results . 66 3.3.1 Breeding success . 66 3.3.2 Survival . 71 3.4 Discussion . 73 References . 78 4 Effect of reciprocal translocations on the genetic structure of two inbred bird populations 83 4.1 Introduction . 84 4.2 Material and methods . 85 4.2.1 Study populations . 85 4.2.2 Population genetic characteristics . 87 4.2.3 Statistical analyses . 90 4.3 Results . 91 4.3.1 Indices of genetic diversity per island population . 92 4.4 Discussion . 97 Appendices 105 A Microsatellite markers and genotyping 107 7 B Effect of heterozygosity on survival to adulthood 111 References . 113 5 Effects of reciprocal translocations on reproductive success, survival, and recruitment in two inbred South Island robin populations 123 5.1 Introduction . 124 5.2 Material and methods . 125 5.2.1 Study populations . 125 5.2.2 Breeding success . 126 5.2.3 Survival and recruitment . 127 5.2.4 Sperm quality . 127 5.2.5 Unhatched eggs . 129 5.2.6 Parental care . 129 5.2.7 Data analyses . 130 5.3 Results . 133 5.3.1 Breeding success . 133 5.3.2 Survival and recruitment . 134 5.3.3 Sperm quality . 134 5.3.4 Unhatched eggs . 137 5.3.5 Parental care . 138 5.3.6 Body mass . 139 5.4 Discussion . 139 Appendices 143 C Paternity assignment 145 D Molecular sex determination 147 8 E Sperm abnormalities and morphometry 149 F Fertility status of unhatched eggs 151 G Incubation attentiveness and nestling provisioning 153 H Results of breeding success analyses 155 I Results of survival and recruitment analyses 161 J Results of sperm analyses 163 K Results of parental care analyses 167 L Results of body mass analyses 169 References . 170 6 Effects of reciprocal translocations on immunocompetence and pathogen loads in two inbred South Island robin populations 179 6.1 Introduction . 180 6.2 Material and methods . 181 6.2.1 Field work and study populations . 181 6.2.2 Phytohaemagglutinin assay . 182 6.2.3 Blood smears . 184 6.2.4 Salmonella and Campylobacter screen . 184 6.2.5 Ectoparasite loads . 186 6.2.6 Statistical analyses . 186 6.3 Results . 189 6.3.1 PHA immune test . 189 6.3.2 Blood smears . 190 6.3.3 Campylobacter screen . 191 9 6.3.4 Ectoparasite loads . 191 6.4 Discussion . ..
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