The genetic effects of bottlenecks and disease in three iconic New Zealand bird species
Studies exploring the genetic consequences of population bottlenecks are increasingly examining the loss of diversity at functional loci (such as genes associated with the immune system), while neutral markers (such as microsatellites) are often used as a basis for general genetic diversity comparisons. Within this field of investigation, aspects that require further research include whether 1) remnant, genetically depauperate mainland and insular-originating source populations differ in immunity-associated genetic diversity, 2) contemporary bottleneck circumstance (i.e. anthropogenic vs. natural) differentially affects the genetic diversity of various molecular markers, and 3) adaptation to novel pathogens can be detected in isolated populations. I investigate these questions using selectively neutral microsatellite markers, the adaptive immunity-associated major histocompatibility complex (MHC), and innate immunity-associated toll-like receptor (TLR) loci in three iconic New Zealand bird species. In a critically endangered parrot, the kakapo (Strigops habroptilus), I have discovered that MHC, but not TLR, loci show similar diversity patterns as neutral markers. I found little diversity within and across two source populations of kakapo for five TLR loci. However, next-generation sequencing of MHC class II B loci revealed unique variants in a recently deceased mainland-originating kakapo and one of his three offspring. I propose that the MHC should be used to rank individuals for breeding opportunity, especially as pedigree methods and diversity data from neutral loci were not able to detect subtle diversity differences among siblings, which may be important for the long-term viability of kakapo as it relates to immunocompetence. In a threatened passerine, the South Island saddleback (Philesturnus carunculatus), I found that contemporary translocation-induced bottlenecks resulted in greater losses of microsatellite than MHC diversity. By comparison, temporal (encompassing a disease-induced bottleneck) fluctuations in diversity were greater for MHC markers than microsatellite loci. Both translocation- and disease-induced contemporary bottlenecks affected TLR diversity to a greater extent than diversity of either microsatellites or MHC. I found significant temporal changes in the frequencies of two TLR1LA alleles (coincident with the pathogen outbreak), but no further change in subsequent years. These alleles differ by a non-conservative amino acid variant that is associated with the pathogen-binding region of TLR1LA, providing support that pathogen-mediated selection has contributed to the observed patterns at TLR1LA. My results indicate that bottleneck circumstance differentially affects genetic diversity across loci. Finally, beak and feather disease virus (BFDV) was detected for the first time in an isolated population of red-crowned parakeets (Cyanoramphus novaezelandiae) in 2008 on Little Barrier Island (Hauturu-o-Toi) in New Zealand. By 2013, the prevalence of the pathogen had significantly decreased. I found evidence for selection at locus TLR3, compared to microsatellites and the MHC, which showed only minor changes or stayed constant across this same time period. An alternative to, or interacting process with, population adaptation to BFDV is fluctuating population density potentially dropping below the threshold for BFDV maintenance. In the face of increased concern over disease outbreaks in wild populations, my results illustrate the ability of natural processes to buffer against disease. Taken together, these studies show that genetic diversity patterns across loci reflect the species-specific narratives of population decline. In addition, because variability in the genetic diversity of historically bottlenecked species can still be detected across loci, I emphasize the importance of continued discussion surrounding genetic management of threatened organisms thought to be a "lost cause" due to severe population bottlenecks or very low neutral genetic diversity.
Advisor: Robertson, Bruce; Jamieson, Ian
Degree Name: Doctor of Philosophy
Degree Discipline: Zoology
Publisher: University of Otago
Keywords: MHC; TLR; South Island saddleback; kakapo; red-crowned parakeet; immunogenetics; conservation genetics; population genetics; molecular ecology; pathogen-mediated selection
Research Type: Thesis