Contrasting genomic consequences of anthropogenic reintroduction and natural recolonisation in high-arctic wild reindeer

Anthropogenic reintroduction can supplement natural recolonisation in reestablishing a species distribution and abundance. However, both reintroductions and recolonisations can give rise to population bottlenecks that reduce genetic diversity and increase inbreeding, potentially causing accumulation of genetic load and reduced fitness. Most current populations of the endemic high-arctic Svalbard reindeer (Rangifer tarandus platyrhynchus) originate from recent reintroductions or recolonisations following regional extirpations due to past overharvesting. We investigated and compared the genomic consequences of these two paths to reestablishment using whole-genome shotgun sequencing of 100 Svalbard reindeer across their range. We found little admixture between reintroduced and natural populations. Two reintroduced populations, each founded by 12 individuals around four decades (i.e. 8 reindeer generations) ago, formed two distinct genetic clusters. Compared to the source population, these populations showed only small decreases in genome-wide heterozygosity and increases in inbreeding and lengths of runs of homozygosity. In contrast, the two naturally recolonised populations without admixture possessed much lower heterozygosity, higher inbreeding, and longer runs of homozygosity, possibly caused by serial population bottlenecks and/or fewer or more genetically related founders than in the reintroduction events. Naturally recolonised populations can thus be more vulnerable to the accumulation of genetic load than reintroduced populations. This suggests that in some organisms even small-scale reintroduction programs based on genetically diverse source populations can be more effective than natural recolonisation in establishing genetically diverse populations. These findings warrant particular attention in the conservation and management of populations and species threatened by habitat fragmentation and loss.