Comparative analyses of olfactory receptor repertoires reveal evolutionary dynamics and adaptation of freshwater and seawater gobies based on the chromosome-level genomes

The olfactory receptor (OR) genes underpin vertebrates' detection of environmental chemical signals; the expansion, functional differentiation, and genomic diversity of the OR gene family drive niche adaptation. Aquatic OR genes evolve in response to salinity and odorant spectra to maintain olfactory adaptability, shaping distinct olfactory traits in freshwater and seawater fish. To explore OR gene evolution linked to salinity adaptation, we systematically identified and analyzed the OR genes of three freshwater and four seawater gobiid species (Perciformes, Gobiidae) at the chromosome-level genomes. The analysis of the OR gene composition of gobies revealed significant habitat-related differentiation: the seawater gobiid species exhibited a higher average number of OR genes (115.50) compared to the freshwater gobiid species (89.67). This distribution pattern indicated an adaptive expansion of the OR gene family to accommodate the more complex chemical signaling environment in seawater habitats. Sequence analysis of the conserved motifs of the OR gene confirmed that the conserved motifs across different gobies exhibited similar sequence compositions, underscoring the evolutionary conservation of the OR gene sequence during adaptive evolution. Phylogenetic analysis of the OR gene families (ζ, η, δ, ε) demonstrated a distinct habitat-specific distribution pattern among gobiid species: the ε family was consistently present in seawater gobiid species but absent in freshwater gobiid species, whereas the η family maintained a dominant proportion in both seawater and freshwater gobiid species. A comparative analysis of the OR gene subfamilies identified a total of 89 OR gene subfamilies among freshwater and seawater gobiid species. Of these, 38 subfamilies were unique to freshwater gobiid species, while 67 subfamilies were exclusively found in four seawater gobiid species. Chromosome-level genomic analysis indicated that OR genes were not randomly distributed throughout the genome but were organized in clusters, forming gene clusters. Our findings about the changes in the OR gene family associated with habitat divergence in gobiid species would provide new insights into the olfactory adaptation in fish.