Chromosome-scale genome assembly and conservation genomics reveals purifying selection and adaptation in a critically endangered bird

The effective purging of deleterious mutations in small populations can alleviate inbreeding depression caused by historical bottlenecks. However, how evolutionary history and adaptation have influenced the genetic load and genomic make-up in small populations remains contentious. Here, we evaluated the genetic consequences of long-term severe bottlenecks on genetic diversity, genetic load, and adaptation by a critically endangered nocturnal species, the White-eared Night-Heron Gorsachius magnificus (GOM). We assembled a chromosome-scale genome of GOM and applied several conservation genomic analyses on multiple individuals of GOM and its closely related Black-crowned Night-heron Nycticorax nycticorax (NYN). Our analyses revealed contrasting demographic trajectories between the two species with the sharp population decline since the Pleistocene in GOM, whereas large and relatively stable effective population size in NYN. The severe population bottleneck has resulted in a lower level of genetic diversity and a higher level of inbreeding, which further led to a greater number of runs of homozygosity and the accumulation of deleterious mutations in the GOM population relative to the NYN population. The deleterious alleles with strong negative impacts were effectively purged to mitigate the inbreeding depression during the GOM population contractions. We also identified candidate genes under positive selection and specific eyeball tissue that is involved in immune activity, DNA repair functions, and visual functions, which may be related to of adaptation lifestyle of GOM. Overall, our study sheds light on the endangerment mechanism of an endangered species but also provides an invaluable genomic resource for a poorly studied bird group, the Ardeidae.