Population Decline, Inbreeding and Hybridization Shape the Genetic Vulnerability of a Critically Endangered Seabird.

Many endangered species have been rescued from the brink of extinction, yet their long-term viability remains uncertain due to the prolonged genetic consequences of severe bottlenecks. In particular, the combined effects of inbreeding and hybridization with closely related species remain poorly understood. Using a comparative conservation genomic framework, we investigated these issues in the Chinese crested tern (Thalasseus bernsteini), a critically endangered seabird once presumed extinct but which has increased to approximately 100 individuals over the past two decades and its close relative, the great crested tern (T. bergii). We demonstrate that the Chinese crested tern has experienced ongoing genetic erosion. Its prolonged population decline has intensified genetic drift and reduced the efficiency of purifying selection, resulting in genome-wide accumulation of highly deleterious mutations. Highly inbred individuals also carry significantly more homozygous deleterious mutations than less inbred individuals. In both species, runs of homozygosity (ROH) show a relative enrichment of moderately and weakly deleterious mutations. Even more concerning, we found an enrichment of moderately and weakly deleterious mutations in putatively introgressed regions in both species, suggesting that occasional hybridization may have facilitated the spread of deleterious variants and could potentially compromise long-term fitness. These findings highlight that severe bottlenecks have lasting genomic consequences and that both inbreeding and hybridization can increase the genetic vulnerability of small populations-underscoring the importance of management strategies that promote population growth and sustained genetic monitoring.