Tetrapod V1R-like ora genes in an early-diverging ray-finned fish species: The canonical six ora gene repertoire of teleost fish resulted from gene loss in a larger ancestral repertoire

Abstract

Background: Chemical senses serve a multitude of essential functions across the animal kingdom. Vertebrates employ four GPCR families to detect odors, among them the v1r/ora gene family. The V1R family is known to evolve rapidly in the lobe-finned lineage giving rise to tetrapods, but the homologous ORA family consists of just six highly conserved genes in teleost fish, with direct orthologs in the lobe-finned fish coelacanth. Thus, the teleost repertoire of six canonical ora genes was assumed to be the ancestral feature before the divergence of ray-finned and lobe-finned fish. So far, this hypothesis has not been tested with earlier diverging ray-finned fish. Results: We have newly identified the complete ora gene repertoires of five teleost species, and of spotted gar, a basal ray-finned fish, using thorough data mining and extensive phylogenetic analysis. The genomes of eight further teleost species were re-analyzed for their ORA repertoires. We report that direct orthologs of the six canonical ora genes (ora1-6) were present in all newly analyzed species, with faithfully preserved exon/intron structure and mostly preserved genomic arrangement in symmetric pairs for ora1-4. In four teleost species including medaka and cave fish we observe species-specific gene duplication events. Thus, the ora gene repertoire in teleost fish is not quite as strictly conserved as previously assumed. In fact, the examination of non-synonymous vs. synonymous substitution rates (dN/dS) shows pronounced negative selection in five of the six ora genes, but also rare occurrence of positive selection in ora3 and ora6. Surprisingly, spotted gar possesses beyond the six canonical genes three additional genes, ora7-8b, orthologous to coelacanth genes v1r07-10. No orthologs for these genes were found in teleosts and cartilaginous fish. Conclusions: Early diverging ray-finned fish such as the spotted gar possess several v1r-like genes previously assumed to be restricted to the lobe-finned lineage, but now found to be already present in the most recent common ancestor of lobe- and ray-finned fish. Thus, the presence of just six canonical ora genes in many teleost species is not the ancestral feature of the ray-finned lineage, but caused by loss of two ancestral genes in teleosts.