The Iberian lynx was at the brink of extinction by the year 2000 but has since then, and thanks to intensive conservation measures, gone through a remarkable recovery, providing a much-welcomed and encouraging conservation success story. Genetic issues have probably contributed to the decline in the past, and the genetic management of inbreeding and genetic diversity is likely contributing to its recent recovery. The species was an early adopter of genetic and genomic approaches, and the combination of an extreme decline, an intensive monitoring and management programme and extensive genomic resources and data makes the Iberian lynx an excellent model for conservation genomics. Here, we review how genetic and genomic data have contributed to the knowledge of the species evolutionary and demographic history, the evaluation of the genetic status of the species through time, including historical and ancient data, and how this information has prompted and guided conservation actions. In the process, genomics provided valuable insights into the dynamics of functional variation in bottlenecked populations and the consequences of intraspecific and interspecific admixtures. In more applied terms, the species is subjected to an ambitious genetic monitoring and management programme, covering captive, remnant and reintroduced populations, which has succeeded in improving the genetic status of the species and thereby contributed to its recovery. Current genomic work aims at expanding these contributions with novel genomic resources and data while capitalising on extensive demographic and genealogical data provided by the ongoing non-invasive genetic monitoring programme.

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.

Inbreeding depression and genetic rescue are central themes in conservation biology. Translocation is a tool to assist genetic rescue but is connected to risks. A new study by Quinn et al. used genomic data to evaluate translocations as a potential action in montane red fox, bringing important implications also for other threatened species.

Inbreeding depression has been documented in various fitness traits in a wide range of species and taxa, however, the mutational basis is not yet well understood. We investigate how putatively deleterious variation influences fitness and is shaped by individual ancestry by re-sequencing complete genomes of 37 individuals in a natural arctic fox (Vulpes lagopus) population subjected to both inbreeding depression and genetic rescue. We find that individuals with high proportion of homozygous loss of function genotypes (LoFs), which are predicted to exert a strong effect on fitness, generally have lower lifetime reproductive success and live shorter lives compared with individuals with lower proportion of LoFs. We also find that juvenile survival is negatively associated with the proportion of homozygous missense genotypes and positively associated with genome wide heterozygosity. Our results demonstrate that homozygosity of strongly and moderately deleterious mutations can be an important cause of trait specific inbreeding depression in wild populations, and mark an important step towards making more informed decisions using applied conservation genetics.

Isolation at small population size can reduce individual fitness and impede population growth caused by inbreeding and genetic drift (i.e. inbreeding depression). Inbreeding depression can however be circumvented by gene flow from unrelated individuals through masking of recessive deleterious alleles and contribute to population persistence (i.e. genetic rescue). Studying these processes in natural populations across generations and under fluctuating environmental conditions however comes with major challenges. Several gaps in the knowledge thus remain regarding causes and consequences of inbreeding depression and genetic rescue in the wild. Using long term data on life history traits, combined with traditional population genetics and novel genomic techniques, we explored the dynamics of inbreeding and gene flow in the highly fragmented arctic fox (Vulpes lagopus) population in Sweden. This thesis mainly focused on the southernmost subpopulation (Helagsfjällen), previously documented to suffer from inbreeding depression. Construction of a genetically verified pedigree (Chapter I and II) revealed that gene flow from three outbred male foxes released from a captive breeding station in Norway resulted in genetic rescue, expressed as elevated first year survival and breeding success in immigrant first generation offspring (F1; Chapter I). However, the rescue effect likely only lasted for one single generation, as we found no selective advantage in later descendants of immigrants (Chapter II and IV). Whole genome sequencing of a subset of individuals from the same subpopulation showed that some immigrant F2 and F3 individuals were highly inbred despite the recent outbreeding events (Chapter III). Identification of putative deleterious variation within coding regions suggested that the immigrants introduced a large number of strongly deleterious alleles which were absent from the native gene pool (Chapter IV and V). Expression of the deleterious variation introduced may explain the low persistence of genetic rescue. We also found a negative relationship between the amount of homozygous strongly deleterious mutations and individual fitness (Chapter IV) and may be an important cause of inbreeding depression in the Swedish arctic fox. Finally, when replicating the study of genomic consequences of inbreeding and gene flow, by including an additional Swedish subpopulation (Vindelfjällen) located further north, we found contrasting patterns between the two subpopulations. While inbreeding decreased in both Helagsfjällen and Vindelfjällen following immigration, the proportion of deleterious variation increased in Helagsfjällen but not in Vindelfjällen. A potential explanation could be more regular gene flow between northern located subpopulations compared to the more geographically isolated population in Helagsfjällen, which may instead have purged a subset of strongly deleterious variation pre immigration. The results from this thesis highlight the transient nature of genetic rescue and the importance to study fitness and genetic effects of gene flow across several generations, as immigration could have negative consequences that are not manifested initially. Finally, as the effects of gene flow can be highly context dependent, demographic histories and functional genetic variation in both source and target populations should be considered before making translocation decisions for conservation purposes.

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.

In socially flexible species, the tendency to live in groups is expected to vary through a trade-off between costs and benefits, determined by ecological conditions. The Resource Dispersion Hypothesis predicts that group size changes in response to patterns in resource availability. An additional dimension is described in Hersteinsson's model positing that sociality is further affected by a cost-benefit trade-off related to predation pressure. In the arctic fox (Vulpes lagopus), group-living follows a regional trade-off in resources' availability and intra-guild predation pressure. However, the effect of local fluctuations is poorly known, but offers an unusual opportunity to test predictions that differ between the two hypotheses in systems where prey availability is linked to intra-guild predation. Based on 17-year monitoring of arctic fox and cyclic rodent prey populations, we addressed the Resource Dispersion Hypothesis and discuss the results in relation to the impact of predation in Hersteinsson's model. Group-living increased with prey density, from 7.7% (low density) to 28% (high density). However, it remained high (44%) despite a rodent crash and this could be explained by increased benefits from cooperative defence against prey switching by top predators. We conclude that both resource abundance and predation pressure are factors underpinning the formation of social groups in fluctuating ecosystems.

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.

Reduced fitness through genetic drift and inbreeding is a major threat to small and isolated populations. Although previous studies have generally used genetically verified pedigrees to document effects of inbreeding and gene flow, these often fail to capture the whole inbreeding history of the species. By assembling a draft arctic fox (Vulpes lagopus) genome and resequencing complete genomes of 23 additional foxes born before and after a well-documented immigration event in Scandinavia, we here look into the genomic consequences of inbreeding and genetic rescue. We found a difference in genome-wide diversity, with 18% higher heterozygosity and 81% lower F-ROH in immigrant F1 compared to native individuals. However, more distant descendants of immigrants (F2, F3) did not show the same pattern. We also found that foxes with lower inbreeding had higher probability to survive their first year of life. Our results demonstrate the important link between genetic variation and fitness as well as the transient nature of genetic rescue. Moreover, our results have implications in conservation biology as they demonstrate that inbreeding depression can effectively be detected in the wild by a genomic approach.