Natural and Anthropogenic Drivers of Genomic Diversity in the California Towhee: Conservation Implications for Peripheral Populations

ABSTRACT

Demographic, geographic, and environmental factors such as effective population size, isolation, and habitat availability interact to shape contemporary levels of population genomic diversity. Such factors must be carefully evaluated and contextualized at both the intraspecific and interspecific levels when assessing the conservation status of imperiled species. Here, we studied the population genomics of a perching songbird, the California towhee ( Melozone crissalis ), by generating a high‐quality annotated reference genome assembly (N50 = 22 Mb among 627 contigs, max contig size 89.1 Mb) and conducting whole‐genome resequencing on n  = 81 individual birds sampled from multiple geographic sites across much of the species' range. California towhee sampled from Inyo County and from Southern Oregon, on the periphery of their geographic range, showed reduced heterozygosity and elevated inbreeding compared (a) to other sampled California towhee populations and (b) to related Threatened songbirds. Contemporary effective population sizes ( N _e ) were low for these two peripheral populations, and ancestry patterns of the federally protected Inyo population reveal the remarkably clear genomic signature of a documented, human‐induced demographic bottleneck. Elevated genomic differentiation ( F _ST ) in the Oregon and Inyo populations, ecological niche modeling, and spatial patterns of gene flow all provide strong support for genetic isolation, limited connectivity, and demographic independence. Both peripheral populations show evidence indicative of local adaptation, as gauged by landscape genetic approaches. Our data highlight the tension that exists between the idealistic goal of conserving all the diversity in a gene pool (e.g., isolated peripheral populations that may contain locally adapted variants) versus the less desirable but more practical goal of focusing expensive conservation efforts on the core gene pool.