Chromosome-Level Genome Assembly of the Speckled Blue Grouper (Epinephelus cyanopodus) Provides Insight into Its Adaptive Evolution

SIMPLE SUMMARY: The coral reef-dwelling grouper Epinephelus cyanopodus has huge economic and ecological value. Due to its special reproductive strategy, complex social structure, and classification controversy, this species is a good model to study the coral reef ecosystem and the classification and speciation of groupers. The lack of genomic resources has hampered research into the genetic basis of their biological traits and adaptive evolution. Therefore, we have assembled a high-quality genome of E. cyanopodus and provided insights into the genetic basis of its adaptive evolution and rapid differentiation at the genomic level, as well as a foundation for subsequent studies on mechanisms of speciation, resistance breeding and genetic conservation for this species. ABSTRACT: Epinephelus cyanopodus is a coral reef-dwelling grouper with important economic and ecological value and is widely distributed in the western Pacific Ocean. The lack of genomic resources for E. cyanopodus hinders its adaptive evolution and phylogeny research. We constructed the first high-quality genome of E. cyanopodus based on DNBSEQ, PacBio, and Hic sequencing technologies, with a genome size of 998.82 Mb, contig N50 of 5.855 Mb, and scaffold N50 of 41.98 Mb. More than 99.7% of contigs were anchored to 24 pseudochromosomes, and 94.2% of BUSCO genes were found in the E. cyanopodus genome, indicating a high genome assembly completeness. A total of 26,337 protein-coding genes were predicted, of which 98.77% were functionally annotated. Phylogenetic analysis showed that E. cyanopodus separated from its closely related species Epinephelus akaara about 11.5–26.5 million years ago, and the uplift of the Indo-Australian archipelago may have provided an opportunity for its rapid radiation. Moreover, several gene families associated with innate and adaptive immunity were significantly expanded in speckled blue grouper compared to other teleost genomes. Additionally, we identified several genes associated with immunity, growth and reproduction that are under positive selection in E. cyanopodus compared to other groupers, suggesting that E. cyanopodus has evolved broad adaptability in response to complex survival environment, which may provide the genetic basis for its rapid radiation. In brief, the high-quality reference genome of the speckled blue grouper provides a foundation for research on its biological traits and adaptive evolution and will be an important genetic tool to guide aquaculture and resolve its taxonomic controversies in future studies.