Abstract
Theory predicts that rapid decreases in population size (“population bottlenecks”) will result in initial decreases in allelic diversity through a random sampling of individuals from the source population, followed by subsequent losses through genetic drift (random sampling of alleles from one generation to the next) if population sizes remain small. Years of empirical research based on neutral genetic diversity (i.e. the diversity of alleles or loci for which mutations do not result in changes to fitness) supports this theory. However, it has been argued that selection will maintain diversity at functionally important genes, even through severe bottlenecks. The major histocompatibility complex (MHC) forms an integral component of the vertebrate immune response, and due to strong balancing selection, is one of the most polymorphic regions of the entire genome. Despite 20 years of research in natural populations, empirical studies offer highly contradictory explanations of the relative roles of selection and genetic drift in shaping MHC variation during population bottlenecks. Many studies conclude that “drift outweighs selection”, rendering MHC diversity effectively neutral during population declines, while several others have found evidence that balancing selection can maintain MHC diversity during these events, even while neutral diversity is lost. A few studies have concluded that in small populations, selection can accelerate the rate of loss for adaptive diversity. In this thesis, I test for signals of balancing selection and genetic drift in shaping post-bottleneck MHC diversity, in an effort to inform the debate in this research field. I also examine factors that influence the impact of population bottlenecks, and which may have led to the disparity among previous study results. I focus my research on threatened New Zealand passerines, which provide a model study system due to their bottleneck histories, as well as availability of both pre- and post-bottleneck samples. To achieve my goals, I compare genetic diversity at MHC class II B loci and at microsatellite loci.
I first synthesise the results of previous studies that examined MHC and neutral genetic diversity in bottlenecked populations for multiple vertebrate taxa. Based on meta-analytical techniques, I conclude that bottleneck events generally result in loss of both MHC and neutral genetic diversity, and that MHC diversity can be lost at a faster rate than neutral diversity in natural populations. I find that a key factor in shaping genetic diversity is bottleneck duration, with prolonged bottlenecks resulting in the greatest impacts. In a subsequent chapter, I go on to characterise MHC class II B diversity in contemporary populations of New Zealand South Island and North Island saddlebacks. I find evidence of historic balancing selection, which helps to identify classical MHC allele sequences (under strong selection) from those of non-classical loci (not under strong selection). I also find that South Island saddlebacks have less MHC diversity than North Island saddlebacks, probably due to differing bottleneck histories. In Chapter 5, I examine pre- and post-bottleneck genetic diversity in New Zealand saddlebacks and robins by comparing museum and contemporary samples. The results of this chapter indicate that contemporary samples have less MHC and less microsatellite diversity compared to historic ones, and have lost a greater proportion of MHC variation compared to microsatellite variation. The influence of bottleneck severity is also evident, with South Island saddlebacks having experienced the strongest impacts, and North Island robins being the least impacted. Overall, the results of this thesis suggest that New Zealand’s threatened species are likely to harbour less overall MHC genetic diversity than in the past, and probably less than widespread species elsewhere. It is evident that genetic drift plays a strong role in shaping the MHC diversity present in these populations. For conservation purposes, I suggest that management goals should continue to be aimed at maintaining genome-wide genetic diversity.