Demographic declines have important consequences for population viability, since they can lead to losses in genome diversity, as well as increased inbreeding and expression of deleterious mutations. Scandinavia was colonized by the Arctic fox (Vulpes lagopus) at the Pleistocene/Holocene transition, and the population has since been on the periphery of the global distribution. The Scandinavian population became even more fragmented in the early 1900s due to human persecution, and experienced an additional decline in the 1980s. We generated high-coverage genomes from pre-bottleneck, as well as modern Scandinavian and Russian specimens, and found that genome-wide diversity was lower and inbreeding higher in Scandinavia compared to the Siberian population, even prior to the historical bottleneck, most likely reflecting the long-term partial isolation and recent postglacial origin of the Scandinavian population. The southern subpopulation has the highest inbreeding levels, likely due to having been recently founded and highly isolated. Our results also show that although inbreeding increased substantially over the past century, the amount of total genetic load did not change. Overall, these findings illustrate the utility of a temporal approach to disentangle the genomic consequences of recent declines from ancient biogeographic processes.

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.

Diseases and parasites are important drivers of population dynamics in wild mammal populations. Small and endangered populations that overlap with larger, reservoir populations are particularly vulnerable to diseases and parasites, especially in ecosystems highly influenced by climate change. Sarcoptic mange, caused by a parasitic mite Sarcoptes scabiei, constitutes a severe threat to many wildlife populations and is today considered a panzootic. The Scandinavian arctic fox Vulpes lagopus is endangered with a fragmented distribution and is threatened by e.g. red fox Vulpes vulpes expansion, prey scarcity and inbreeding depression. Moreover, one of the subpopulations in Scandinavia has suffered from repeated outbreaks of sarcoptic mange during the past decade, most likely spread by red foxes. This was first documented in 2013 and then again 2014, 2017, 2019, 2020 and 2021. We used field inventories and wildlife cameras to follow the development of sarcoptic mange outbreaks in this arctic fox subpopulation with specific focus on disease transmission and consequences for reproductive output. In 2013–2014, we documented visual symptoms of sarcoptic mange in about 30% of the total population. Despite medical treatment, we demonstrate demographic consequences where the number of arctic fox litters plateaued and litter size was reduced after the introduction of S. scabiei. Furthermore, we found indications that mange likely was transmitted by a few arctic foxes travelling between several dens, i.e. ‘super-spreaders'. This study highlights sarcoptic mange as a severe threat to small populations and can put the persistence of the entire Scandinavian arctic fox population at risk.

Translocations are a widespread approach to conserve threatened populations. Given the rapid decline and genetic deterioration of many natural populations, translocations are expected to become even more common in the future. The success of translocations is, however, dependent on multiple context-dependent factors, such as demographic and genetic status, habitat quality and animal behaviour. The Scandinavian arctic fox (Vulpes lagopus) exists in a small, fragmented population that is demographically vulnerable and exposed to inbreeding depression. In the early 2000 s, releases of arctic foxes from the Norwegian Captive Breeding Programme were initiated with the purpose of reintroducing populations to formerly inhabited areas and promoting connectivity. Since 2008/2009, 61 foxes have been released in Junkeren, Norway to re-establish an unoccupied area. We used a combination of field observations and microsatellite genotyping from the release site and two neighbouring subpopulations to investigate (i) the probability of establishment and reproduction for released foxes at the release site and in neighbouring subpopulations, and (ii) the impact on litter size and genetic composition in the recipient populations. Results showed that 18% of the released foxes were established at the release site, or in neighbouring subpopulations and 11.5% reproduced successfully. The extent of post-release dispersal into neighbouring subpopulations was also relatively high (11.5%). During the study period, the number of litters more than doubled in the subpopulations with released foxes contributing 29.5% to this increase, but no clear effect of immigration on litter size was found. There was a slight increase in genetic variation in one of the subpopulations, and a significant decline in genetic divergence between subpopulations. We conclude that despite extensive releases, demographic and genetic effects were highly context-dependent. This study highlights the challenges of reinforcement programmes in small populations and reintroductions to unoccupied sites, especially for highly mobile species in a fragmented landscape. 

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.

Genome-wide association studies provide good opportunities for studying the genetic basis of adaptive traits in wild populations. Yet, previous studies often failed to identify major effect genes. In this study, we used high-density single nucleotide polymorphism and individual fitness data from a wild non-model species. Using a whole-genome approach, we identified the MC1R gene as the sole causal gene underlying Arctic fox Vulpes lagopus fur colour. Further, we showed the adaptive importance of fur colour genotypes through measures of fitness that link ecological and evolutionary processes. We found a tendency for blue foxes that are heterozygous at the fur colour locus to have higher fitness than homozygous white foxes. The effect of genotype on fitness was independent of winter duration but varied with prey availability, with the strongest effect in years of increasing rodent populations. MC1R is located in a genomic region with high gene density, and we discuss the potential for indirect selection through linkage and pleiotropy. Our study shows that whole-genome analyses can be successfully applied to wild species and identify major effect genes underlying adaptive traits. Furthermore, we show how this approach can be used to identify knowledge gaps in our understanding of interactions between ecology and evolution.

Genetic rescue can facilitate the recovery of small and isolated populations suffering from inbreeding depression. Long-term effects are however complex and examples spanning over multiple generations under natural conditions are scarce. The aim of this study was to test for long-term effects of natural genetic rescue in a small population of Scandinavian Arctic foxes (Vulpes lagopus). By combining a genetically verified pedigree covering almost 20 years with a long-term dataset on individual fitness (n=837 individuals), we found no evidence for elevated fitness in immigrant F2 and F3 compared to native inbred foxes. Population inbreeding levels showed a fluctuating increasing trend and emergence of inbreeding within immigrant lineages shortly after immigration. Between 0-5 and 6-9 years post immigration, the average population size decreased by almost 22 % and the average proportion of immigrant ancestry rose from 14 % to 27 %. Y chromosome analysis revealed that two out of three native male lineages were lost from the gene pool, but all founders represented at the time of immigration were still contributing to the population at the end of the study period through female descendants. The results highlight the complexity of genetic rescue and suggest that beneficial effects can be brief. Continuous gene flow may be needed for small and threatened populations to recover and persist in a longer time perspective.

The Arctic fox (Vulpes lagopus) population in Fennoscandia experienced a drastic bottleneck in the late 19th century as a result of high hunting pressure. In the 1990s, despite nearly 70 years of protection, the population showed no signs of recovery. In order to mitigate the population decline and facilitate re-establishment, conservation actions including supplementary feeding and red fox culling were implemented in 1998, followed by the reintroduction of foxes from a captive breeding programme, starting in 2006. A positive demographic impact of these actions is evident from a doubling of the population size over the past decade. We used genetic data collected in eight subpopulations between 2008 and 2015 to address whether the recent demographic recovery has been complemented by changes in genetic variation and connectivity between subpopulations. Our results show that genetic variation within subpopulations has increased considerably during the last decade, while genetic differentiation among subpopulations has decreased. A marked shift in metapopulation dynamics is evident during the study period, suggesting substantially increased migration across the metapopulation. This shift followed the recolonization of an extinct subpopulation through the release of foxes from the captive breeding programme and was synchronized in time with the implementation of supplementary feeding and red fox culling in stepping stone patches between core subpopulations in mid-Scandinavia. Indeed, the increase in genetic variation and connectivity in the Scandinavian arctic fox population suggests that metapopulation dynamics have been restored, which may indicate an increase in the long-term viability of the population.

Isolation of small populations can reduce fitness through inbreeding depression and impede population growth. Outcrossing with only a few unrelated individuals can increase demographic and genetic viability substantially, but few studies have documented such genetic rescue in natural mammal populations. We investigate the effects of immigration in a subpopulation of the endangered Scandinavian arctic fox (Vulpes lagopus), founded by six individuals and isolated for 9 years at an extremely small population size. Based on a long-term pedigree (105 litters, 543 individuals) combined with individual fitness traits, we found evidence for genetic rescue. Natural immigration and gene flow of three outbred males in 2010 resulted in a reduction in population average inbreeding coefficient (f), from 0.14 to 0.08 within 5 years. Genetic rescue was further supported by 1.9 times higher juvenile survival and 1.3 times higher breeding success in immigrant first-generation offspring compared with inbred offspring. Five years after immigration, the population had more than doubled in size and allelic richness increased by 41%. This is one of few studies that has documented genetic rescue in a natural mammal population suffering from inbreeding depression and contributes to a growing body of data demonstrating the vital connection between genetics and individual fitness.

Understanding the response of boreal species to past climate warming can help to predict future responses to climate change. In the Northern Hemisphere, the distribution and abundance of northern populations have been influenced by previous glaciations. In this study, we investigated the population history of the Fennoscandian red fox (Vulpes vulpes), which is a generalist carnivore currently undergoing range expansion in the tundra ecosystem. By analysing a 696 bp sequence of the mitochondrial DNA (N = 259) and two Y chromosome-specific microsatellite loci (N = 120), we specifically investigated where the red fox survived the Last Glacial Maximum and how Fennoscandia was recolonized. There was high genetic continuity across most of Fennoscandia, and we identified at least two recolonization pathways: one from continental Europe and one from the northeast (Siberia). Mitochondrial haplotype diversity displayed a significant decline with increasing latitude, consistent with expectations of unidirectional colonization. Each region displayed signatures of recent demographic and/or range expansions. For Finland, an additional recolonization route was suggested from the mismatch distribution analysis and identification of novel haplotypes. We concluded that, as with many boreal generalist species, the Fennoscandian red fox originates from multiple refugia, suggesting that it has benefited from diverse evolutionary histories, potentially enhancing its tolerance to different habitat conditions.