Recent and Historical Determinants of Genomic Erosion by Structural Variation and SNPs Across a Pan-Holarctic Superspecies

Despite disproportionate fitness impacts imposed by deleterious structural variants (SVs) and associated transposable elements, few studies have yet examined their relative contribution to genomic erosion. To examine the role of both recent and ancient population history in the accumulation of deleterious SVs relative to single nucleotide polymorphisms (SNPs), the rock and willow ptarmigan (Lagopus spp.) superspecies form an ideal pan-Holarctic system, harbouring a broad range of historical effective population sizes increasingly threatened by fragmentation and climate change. By contrasting diversity ratios for non-synonymous SNPs and non- neutral SVs across 99 individuals from 12 island and mainland populations, we find that purifying selection against most putatively deleterious SVs appears insufficient to prevent their long-term accumulation in small populations, conforming with classic nearly-neutral dynamics. Likewise, proportions of realised (homozygous), masked (heterozygous) and fixed drift load due to putative highly and mildly deleterious SVs mirrored SNPs in mostly accumulating as a function of increased homozygosity in smaller populations. However, population-specific differences in the accrual of drift debt due to SVs did not reflect historical Ne alone: elevated realised load but reduced drift load in the Pyrenees (relative to the smallest population; Svalbard) indicate that the effects of recent fragmentation-induced inbreeding have yet to fully manifest. Our findings highlight the need to account for recent population decline and fragmentation, rather than solely relying on historical Ne to predict outcomes of genomic erosion— especially given the potential for disproportionate drift debt imposed by deleterious SVs.