Structural genomic variation in the inbred Scandinavian wolf population contributes to the realized genetic load but is positively affected by immigration

When populations decrease in size and may become isolated, genomic erosion
by loss of diversity from genetic drift and accumulation of deleterious
mutations is likely an inevitable consequence. In such cases, immigration
(genetic rescue) is necessary to restore levels of genetic diversity and
counteract inbreeding depression. Recent work in conservation genomics
have studied these processes focusing on genetic diversity of single
nucleotide polymorphisms. In contrast, our knowledge about structural
genomic variation (insertions, deletions, duplications and inversions) in
endangered species is limited. We analysed whole-genome, short-read
sequences from 212 wolves from the inbred Scandinavian population, and
from neighbouring populations in Finland and Russia, and detected
>35,000 structural variants (SVs) after stringent quality and
genotype frequency filtering; >26,000 high-confidence variants
remained after manual curation. The majority of variants were shorter than
1 kb, with a distinct peak in the length distribution of deletions at 190
bp, corresponding to insertion events of SINE/tRNA-Lys elements. The site
frequency spectrum of SVs in protein-coding regions was significantly
shifted towards rare alleles compared to putatively neutral variants,
consistent with purifying selection. The realized genetic load of SVs in
protein-coding regions increased with inbreeding levels in the
Scandinavian population, but immigration provided a genetic rescue effect
by lowering the load and reintroducing ancestral alleles at loci fixed for
derived SVs. Our study shows that structural variation comprises a common
type of in part deleterious mutations in endangered species and that
establishing gene flow is necessary to mitigate the negative consequences
of loss of diversity.