Genomic health is dependent on long‐term population demographic history

Abstract

Current genetic methods of population assessment in conservation biology have been challenged by genome-scale analyses due to their quantitatively novel insights. These analyses include assessments of runs-of-homozygosity (ROH), genomic evolutionary rate profiling (GERP), and mutational load. Here, we aim to elucidate the relationships between these measures using three divergent ungulates: white-tailed deer, caribou, and mountain goat. The white-tailed deer is currently expanding, while caribou are in the midst of a significant decline. Mountain goats remain stable, having suffered a large historical bottleneck. We assessed genome-wide signatures of inbreeding using the inbreeding coefficient F and %ROH (F-ROH) and identified evolutionarily constrained regions with GERP. Mutational load was estimated by identifying mutations in highly constrained elements (CEs) and sorting intolerant from tolerant (SIFT) mutations. Our results showed that F and F-ROH are higher in mountain goats than in caribou and white-tailed deer. Given the extended bottleneck and low N-e 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 and the lowest dN/dS values, both of which are indicative of greater purifying selection; this is also 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, in addition to dN/dS, while caribou were intermediate. Our results demonstrate that extended bottlenecks may lead to reduced diversity and increased F-ROH in ungulates, but not necessarily an increase in mutational load, probably due to the purging of deleterious alleles in small populations.