The population genetics of a chromosomal inversion linked to social behavior in the white-throated sparrow (Zonotrichia albicollis )

The field of population genetics broadly addresses how genetic diversity in natural populations is generated, shaped and maintained. In this dissertation, I use a population genetic approach to understand the evolution of a chromosomal inversion that influences coloration, social behavior and mate choice in the white-throated sparrow (Zonotrichia albicollis). White-striped sparrows (WS) are heterozygous for the ZAL2m inversion and are more territorially and sexually aggressive than tan-striped sparrows (TS). TS do not have the inversion, invest more in parental care and are less likely to seek extra-pair copulations. The plumage morphs occur at approximately equal frequency and the ZAL2m inversion is maintained in the population through an exceptionally strong pattern of disassortative mating where almost all breeding pairs are TS x WS. We used targeted sequencing to survey SNPs on the standard chromosome, ZAL2, and the ZAL2m. We found that the inversion completely suppresses recombination between the homologous chromosomes, except in the short distal region outside of the polymorphism. This results in exceptional linkage disequilibrium, genetic structure and high divergence, and suggests that the ZAL2m is a rare example of a long-term balanced polymorphism. To understand these patterns in the context of the rest of the genome, we sequenced loci from other autosomes, as well as the ZW sex chromosomes. We describe a strong negative correlation between genetic diversity and chromosome size, which is highly varied in avian genomes. Genetic variation is greatly reduced on the ZAL2 and ZAL2 m chromosomes relative to other similarly sized chromosomes and sex chromosome variation is also exceedingly low. We hypothesize that the low diversity observed for the ZAL2/ZAL2m and sex chromosomes results from the increased sensitivity to natural selection and genetic drift associated with regions of low recombination. Finally, we identified and characterized polymorphisms in candidate genes that could underlie the social behaviors associated with the inversion. In summary, our data offer insights into the molecular evolution and maintenance of inversions, empirical evidence supporting the relationship between chromosome size and diversity and a set of candidate polymorphisms that could influence social behavior the white-throated sparrow.