Inbreeding depression by polygenic load following a severe population bottleneck

It is poorly understood how populations survive extreme bottlenecks despite severe inbreeding. We investigate the genomic architecture of inbreeding in the once critically endangered Seychelles warbler (Acrocephalus sechellensis) using 37 years of individual-based monitoring and 1.8 million SNPs. Linkage disequilibrium patterns reveal a historical effective population size of ~270 that plummeted to ~13 coinciding with human colonisation events of the Seychelles archipelago. Contemporary genomes are over one-third inbred from recent inbreeding measured by runs of homozygosity (ROH) formed since human colonisation of the Seychelles, 50 generations ago (mean FROH < 50 generations ago = 0.38), and we identify significant inbreeding depression across cross key fitness traits. On average, a 17.9% reduction in lifespan and a 15.1% reduction in lifetime offspring production were associated with each 10% increase in individual inbreeding. Genome-wide scans reveal this depression is caused by a polygenic load. Our results suggest that a history of small population size could have facilitated the selective purging of severe genetic load, while mildly deleterious alleles escaped selection via drift. A partitioned genetic load architecture potentially enabled species recovery despite the inbreeding depression that followed near-extinction.