Comparative Analysis Reveals the Adaptive Evolution of Olfactory System in the Swamp Eel (Monopterus albus) Based on the Chromosome-Level Genome.

The swamp eel (Monopterus albus), known for its benthic and nocturnal feeding habits, exhibits a keen sense of smell. To date, the genomic basis for its adaptive evolution of olfactory system was poorly investigated. In this study, we performed comparative genomic analysis to reveal the evolutionary processes underlying the expansion and diversification of olfactory receptor (OR) genes in the swamp eel. A total of 629 gene families were identified to expand in the swamp eel, with five (OLFR, GNAL, PRKG1, NCALD, and PDE1) distributed in olfactory transduction (KEGG map04740). GO enrichment analysis of these expanded gene families showed biological processes related to sensory perception of smell and detection of chemical stimulus. Among the 287 positively selected genes (PSGs) in the swamp eel, LRRK2, ANKDD1B, APLNR2, SPRED1, AFAP1L2, PLEK2, and PREX2 were linked to signal transduction. A total of 318 OR genes (289 functional genes, 10 partial genes, and 19 pseudogenes) were annotated in the swamp eel genome, significantly surpassing other fish species. Clusters of OR genes were detected on chromosome 4, chromosome 8, chromosome 9, and chromosome 12 in the swamp eel, sharing the same transcriptional orientation, which indicated that tandem duplication was a possible mechanism for the OR gene expansion. Phylogenetic analysis revealed the obvious expansion pattern of OR genes in groups δ and ζ for the swamp eel. Conserved motifs were detected in the OR genes, which indicated the similar functions of OR genes. Our findings unveiled the genomic basis for the olfactory evolution in the swamp eel, providing insights for a better understanding of swamp eel's environmental adaptation and contributing to further investigation of olfactory function in fish. This study enriches the genomic research on the olfactory system of benthic nocturnal fishes and provides a useful evolutionary case for understanding olfactory adaptation to ecological niches in fish.