Comparative and Population Genomics of Host-Pathogen Co-Evolution in Birds

Abstract

Infectious disease produces some of the strongest selective forces on natural populations across the tree of life. The signatures of pathogen-mediated evolution on host genomes have been described for several traditional model organisms, but few studies of more diverse organisms have detected such signatures beyond candidate immune loci. In my dissertation, I combine population and comparative genomics to study the dynamics of pathogen-mediated selection at two evolutionary timescales in wild bird populations. In Chapters 1 and 2, I integrate geographic and temporal sampling to compare the impacts on genomic variability of recent founder events and an epizootic on the House Finch (Haeomorhous mexicanus). House Finches, native to the western US and Mexico, were introduced to the Hawaiian Islands in 1870 and separately to the eastern US in 1940. In 1994, Mycoplasma gallisepticum (MG), previously associated with poultry, jumped to House Finches and caused severe declines. In Chapter 1, I genotype ~2,000 loci in samples collected before and 10 years after the epizootic. I demonstrate that demographic shifts brought about by the founder events have much more profound genomic impacts than pathogen-mediated natural selection. In Chapter 2, I use whole-genome resequencing data in six House Finch populations from three time points. I show that the expansion of the western US population following the last glacial maximum had the largest impact on patterns of genomic variation, followed by the eastern founder event. This genome-wide dataset also enables me to detect a decrease in genetic diversity immediately following the epizootic. Additionally, the lack of temporal differentiation at individual SNPs suggests that House Finches evolved resistance through polygenic selection. As a complement to these population-level analyses, in Chapter 3, I use over 11,000 well-annotated genes from 39 bird genomes to I show that immune genes encoding proteins that interact directly with pathogens consistently show evidence of positive selection. Using a dataset comprised of all genes regardless of function, I also show that immune system functional pathways are enriched for signatures of positive selection. Taken together, I demonstrate that host-pathogen interactions play an important role in shaping the bird genome over long evolutionary timescales.