Dynamics of inbreeding and genetic rescue in a small population

Abstract

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