Elevated recessive lethal frequencies drive hatching failure following near extinction in 'Alalā, the Hawaiian crow

Near-extinction events impose severe genomic bottlenecks that can have lasting fitness consequences, yet the specific mechanisms involved remain poorly understood. 'Alalā, the endemic Hawaiian crow, narrowly avoided extinction when a conservation breeding program was founded from just nine individuals. Although the breeding program has since recovered to ~120 birds, it remains plagued by egg hatching failure rates >50%. To investigate the impacts of this bottleneck on hatching failure and other fitness components, we generated a chromosome-level reference genome and resequenced 175 individuals, including 78 deceased embryos. Although long runs of homozygosity (ROH) >1Mb are abundant in 'Alalā (mean FROH=0.32), associations between FROH and measures of survival and reproduction, including egg failure, were weak or nonexistent. Instead, we identify two recessive lethal haplotypes that together account for ~20% of all hatching failures and have persisted in the population at high frequency (15-25%), hinting at impaired purifying selection. Eco-evolutionary simulation models demonstrate that these limited impacts of ROH and elevated recessive lethal allele frequencies are expected for a species that has endured a severe population bottleneck and exhibits modest levels of non-ROH heterozygosity. Our findings suggest that elevated recessive allele frequencies may be a broadly important consequence of population bottlenecks.