The arctic fox (Vulpes lagopus) is a cold-adapted carnivore with a circumpolar distribution across most Arctic regions. With a remarkable dispersal capacity, the species has been documented moving distances of up to 4,000 km across sea-ice. As contemporary climate change threatens these dispersal routes through continued sea-ice loss, understanding how arctic foxes responded to past climatic fluctuations is increasingly important. The Late Pleistocene was characterized by pronounced climatic oscillations, during which several cold-adapted species failed to track suitable habitat northwards as ice sheets retreated. Mitochondrial evidence suggests that this may also have been the case for arctic foxes. However, given their exceptional dispersal ability, questions remain regarding whether Late Pleistocene southern populations contributed to the arctic fox’s present-day gene pool. Here, we analyze whole genome data from six Eurasian arctic fox specimens dating to the Late Pleistocene alongside 42 modern genomes to investigate demographic processes during this pivotal period. Our results are consistent with a large, genetically connected population across Eurasia with limited population structure during the Late Pleistocene. Although we find no evidence for direct continuity of Late Pleistocene lineages into modern populations, the data support the persistence of a connected population resilient to climatic fluctuations. We further suspect a substantial bottleneck at the transition to the Holocene, consistent with the loss of mitochondrial diversity alongside the retention of autosomal variation. Together, these findings suggest that historical resilience to climatic change was facilitated by extensive population connectivity, whereas increasing isolation of contemporary populations may reduce their capacity to respond to future environmental change.

Accelerating climate change is causing severe habitat fragmentation in the Arctic, threatening the persistence of many cold-adapted species. The Scandinavian arctic fox (Vulpes lagopus) is highly fragmented, with a once continuous, circumpolar distribution, it struggled to recover from a demographic bottleneck in the late 19th century. The future persistence of the entire Scandinavian population is highly dependent on the northernmost Fennoscandian subpopulations (Scandinavia and the Kola Peninsula), to provide a link to the viable Siberian population. By analyzing 43 arctic fox genomes, we quantified genomic variation and inbreeding in these populations. Signatures of genome erosion increased from Siberia to northern Sweden indicating a stepping-stone model of connectivity. In northern Fennoscandia, runs of homozygosity (ROH) were on average ~1.47-fold longer than ROH found in Siberia, stretching almost entire scaffolds. Moreover, consistent with recent inbreeding, northern Fennoscandia harbored more homozygous deleterious mutations, whereas Siberia had more in heterozygous state. This study underlines the value of documenting genome erosion following population fragmentation to identify areas requiring conservation priority. With the increasing fragmentation and isolation of Arctic habitats due to global warming, understanding the genomic and demographic consequences is vital for maintaining evolutionary potential and preventing local extinctions.

Humans have relied on animal fur for centuries, yet fur farming only began recently during the mid-19th Century. Little is known about this incipient domestication or the genomic processes involved. Domestication may involve founder effects, population bottlenecks and low population size, which, when combined with intense artificial selection, lead to inbreeding, a limited gene pool and reduced fitness. The arctic fox (Vulpes lagopus) has been farmed intensively since the early 1900s and has been artificially selected for economic phenotypes. We investigated the origin of these lineages and the genomic consequences of intensive farming by comparing the genomes of farmed and wild arctic foxes from across their range. Our research indicates recent inbreeding through long Runs of Homozygosity and reduced genomic variation in farmed foxes relative to their respective wild populations. We identified a coastal ecotype origin for all Fennoscandian farmed arctic foxes, aligning them phylogenetically with the wild Icelandic population, a geographically isolated and phenotypically distinct coastal lineage. The depleted genome-wide heterozygosity and increased recent inbreeding in farmed fox lineages is consistent with a heavy consequence of domestication, shedding light on the demographic history and genomic consequences of human manipulation. We highlight the need for increased genomic investigations into fur farm populations to understand the incipient domestication process and uncover the cost of intense farming. The genomic consequences of domestication must be considered in the management of fur farms, with actionable steps needed to prevent descendants of escaped farmed foxes from polluting the gene pool in the wild through introgression.

Humans have altered animal lineages by harnessing evolution to suit anthropogenic needs, domesticating wild species. Some domestic populations can persist outside these environments and readily survive in the wild as feral populations. In several systems, lasting consequences have been observed where introgression from domestic populations has diluted unique wild lineages with non-native alleles. This raises key questions regarding what domesticated individuals introduce into wild populations and whether such introgression has fitness consequences. Here, we quantify levels of introgression from farmed foxes (n = 38) into the wild Fennoscandian arctic fox population (n = 1,892), an endangered population that was nearly hunted to extinction at the turn of the 20th century and in which farmed fox–wild hybrids have previously been detected. We assess the effects of farmed fox ancestry on fitness in the Swedish arctic fox population and to identify subpopulations that may be at risk and could benefit from increased gene flow from populations unaffected by farmed fox ancestry. We detected generally low signals of introgression, consistent with historical admixture several generations ago. Based on the Swedish dataset, farmed fox ancestry was associated with reduced juvenile survival (n = 602) and increased adult longevity (n = 115), suggesting potential fitness trade-offs. These results are relevant for conservation management of this vulnerable population and highlight the value of low‑cost genotyping approaches for large‑scale screening of introgression and its ecological consequences, as well as its applications for avoiding introgressed foxes in the captive breeding program and future in situ management.