Genomic health is dependent on population demographic history

Current genetic methods of population assessment in conservation biology have been challenged with genome-scale data, particularly by the quantitatively novel insights provided by genome-wide analyses. These include assessments of runs-of-homozygosity (ROH), genomic evolutionary rate profiling (GERP), and mutational load, all of which are direct measures of genomic health. Here, we aim to elucidate the relationships between these measures and assess the genomic health of three divergent ungulates: the white-tailed deer, caribou, and mountain goat. The white-tailed deer is currently expanding following near extirpation, while caribou are in the midst of a significant decline. Mountain goats remain stable after a large historical bottleneck. We assessed genome-wide signatures of inbreeding using the inbreeding coefficient F and % ROH (FROH) and identified evolutionarily constrained regions with GERP. Mutational load was estimated by identifying mutations in highly constrained elements (CEs) and by sorting intolerant from tolerant (SIFT) mutations. Our results show that F and FROH are significantly higher in mountain goats than in caribou and white-tailed deer. Given the extended bottleneck and low Ne of the mountain goat, this supports the idea that the genome-wide effects of demographic change take time to accrue. Similarly, we found that mountain goats possess more highly constrained CEs which are indicative of greater purifying selection. This is further reflected by fewer mutations in CEs and deleterious mutations identified by SIFT. In contrast, white-tailed deer presented the highest mutational load with both metrics. Our results demonstrate that extended bottlenecks may lead to reduced diversity and increased FROH in ungulates, but not necessarily the accumulation of deleterious alleles. This may be due to the purging of deleterious alleles in small populations. This study empirically demonstrates the relationships between different measures of genomic health in ungulates and highlights the need to consider multiple genomic health metrics during conservation assessments.