An empirical assessment of genomic health in three divergent ungulates: Testing a conservation genetics paradigm

Background/Question/Methods

The unprecedented loss of global biodiversity necessitates informative metrics for conservation biology. Current methods of assessment in conservation genetics have been under debate, but empirical studies have shown that genome-wide assessments can provide quantitatively novel insight over previous methods. These include assessments of runs-of-homozygosity (ROH), genomic evolutionary rate profiling (GERP), and mutational load, all of which are critical measures of genomic health for small populations of conservation concern. The relationships between these measures and conservation status, diversity, and effective population size (Ne), however, are controversial and at-times counter to theoretical expectation. Here, we analysed signatures of genomic health across the ranges of three divergent ungulates to elucidate these relationships. The caribou (Rangifer tarandus) is currently experiencing a significant population decline resulting in low diversity and extremely low Ne. The white-tailed deer (Odocoileus virginianus), in contrast, is expanding and has accordingly high diversity and Ne. The mountain goat (Oreamnos americanus) has recently undergone a massive bottleneck but has since remained stable which has led to intermediately low diversity and Ne. For each, we assessed genome-wide signatures of inbreeding using F and FROH and identified evolutionarily constrained regions with GERP. Mutational load was estimated by identifying mutations in highly constrained elements (CEs).

Results/Conclusions

Our results show that F and FROH are significantly higher in mountain goats than in caribou and white-tailed deer. ROHs in mountain goat are also significantly longer and more numerous. This supports the idea that the genome-wide effects of demographic change take time to accrue, and the length of the bottleneck is responsible for the difference between species. Similarly, we found that mountain goats possess significantly longer and more highly constrained CEs which are indicative of greater purifying selection. This is further reflected by significantly fewer mutations in CEs and genome-wide missense mutations. Our results demonstrate that extended bottlenecks may lead to reduced diversity and increased FROH in ungulates, but not the accumulation of deleterious alleles. This is likely 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 mutational load during conservation assessment.