Pangolin museum genomics reveal the dynamic genetic consequences and extinction risk of the critically endangered Chinese pangolin

Abstract Human-driven biodiversity loss, intensified by illegal hunting and trafficking, has caused severe wildlife population declines and extinctions, necessitating studies on long-term genomic erosion to inform conservation strategies. While temporal genomic analyses using ancient and historical/museum DNA reveal generational impacts, sparse sampling often limits insights into prolonged declines, highlighting the need for time-resolved studies to understand sequential population decline and species persistence under sustained pressures. The Chinese pangolin (Manis pentadactyla), critically endangered as a result of historical overexploitation, has experienced severe continuous population decline pre-1979, 1980-1999, and post-2000. However, the temporal genetic consequences and associated extinction risks remain poorly understood. We analyzed 228 pangolin genomes (133 newly sequenced), spanning continuous population decline, to assess the dynamics of genomic erosion. Our results demonstrate that persistent population decline drive long-term genetic decline within populations, with the severity of population decline correlating directly with the degree of negative genetic impact (e.g., reduced diversity, increased inbreeding and genetic load) and extinction risk. Counterintuitively, however, between populations, those experiencing the most severe population decline (e.g., southwest China) exhibited less extreme relative genetic consequences compared to less severe population decline (e.g., south China), suggesting a stronger dependence on history effective population size before population decline. Critically, the contemporary south China population shows significantly lower genetic diversity, higher inbreeding, elevated genetic load, and consequently higher extinction risk, demanding urgent prioritization for conservation. This study provides novel insights into the complex genomic legacy of continuous population decline, elucidating anthropogenic impacts on genetic erosion and offering a scientific framework for targeted conservation strategies.