Genomic legacy of migration in endangered caribou

Wide-ranging animals, including migratory species, are significantly threatened by the effects of habitat fragmentation and habitat loss. In the case of terrestrial mammals, this results in nearly a quarter of species being at risk of extinction. Caribou are one such example of a wide-ranging, migratory, terrestrial, and endangered mammal. In populations of caribou, the proportion of individuals considered as “migrants” can vary dramatically. There is therefore a possibility that, under the condition that migratory behavior is genetically determined, those individuals or populations that are migratory will be further impacted by humans, and this impact could result in the permanent loss of the migratory trait in some populations. However, genetic determination of migration has not previously been studied in an endangered terrestrial mammal. We examined migratory behavior of 139 GPS-collared endangered caribou in western North America and carried out genomic scans for the same individuals. Here we determine a genetic subdivision of caribou into a Northern and a Southern genetic cluster. We also detect >50 SNPs associated with migratory behavior, which are in genes with hypothesized roles in determining migration in other organisms. Furthermore, we determine that propensity to migrate depends upon the proportion of ancestry in individual caribou, and thus on the evolutionary history of its migratory and sedentary subspecies. If, as we report, migratory behavior is influenced by genes, caribou could be further impacted by the loss of the migratory trait in some isolated populations already at low numbers. Our results indicating an ancestral genetic component also suggest that the migratory trait and their associated genetic mutations could not be easily re-established when lost in a population.Author summary: Genetic determination of migration has not previously been studied in an endangered terrestrial mammal. The use of global positioning system (GPS) transmitters permitted the detection of migratory or sedentary movements of 139 endangered caribou. The presence of both migratory and resident phenotypes in sympatry allowed for us to examine genomic differences among individuals that had experienced similar environments prior to the initiation of migration. In this study, we genotyped 139 caribou using RAD sequencing, and used these genotypes to assess population structure and investigate potential genetic associations with migration. We detected >50 SNPs associated to migration. These SNPs were found in genes with hypothesized roles in determining migration in other organisms. In addition, propensity to migrate depended upon the proportion of Northern or Southern ancestry in individual caribou, and thus on the evolutionary history of its migratory and sedentary subspecies dating back to the last glaciation. We believe that our concerns for the loss of migration in caribou are transferable to other species and systems where there are documented declines, and migration is likewise associated with genes. If–as we reported–migratory behavior is determined by ancestral genes, species could be further impacted, possibly by the loss of the migratory trait in some populations already at low numbers. This loss could perhaps be averted with the maintenance of critical seasonal habitats within and between seasonal ranges.