Bemis, K. E. | bioRxiv Science

bioRxiv2021

Coevolution of the olfactory organ and its receptor repertoire in ray-finned fishes

Ray-finned fishes (Actinopterygii) perceive their environment through a range of sensory modalities, including olfaction 1,2. Anatomical diversity of the olfactory organ suggests that olfaction is differentially important among species 1,3,4. To explore this topic, we studied the evolutionary dynamics of the four main gene families (OR, TAAR, ORA/VR1 and OlfC/VR2) 5 coding for olfactory receptors in 185 species of ray-finned fishes. The large variation in the number of functional genes, between 28 in the Ocean Sunfish Mola mola and 1317 in the Reedfish Erpetoichthys calabaricus, is the result of parallel expansions and contractions of the four main gene families. Several ancient and independent simplifications of the olfactory organ are associated with massive gene losses. In contrast, polypteriforms, which have a unique and complex olfactory organ, have almost twice as many olfactory receptor genes as any other ray-finned fish. These observations suggest a functional link between morphology of the olfactory organ and richness of the olfactory receptor repertoire. Further, our results demonstrate that the genomic underpinning of olfaction in ray-finned fishes is heterogeneous and presents a dynamic pattern of evolutionary expansions, simplifications and reacquisitions.

evolutionary biology↗

bioRxiv2021

Evolutionary dynamics of the OR gene repertoire in teleost fishes: evidence of an association with changes in olfactory epithelium shape

Teleost fishes perceive their environment through a range of sensory modalities, among which olfaction often plays an important role. Richness of the olfactory repertoire depends on the diversity of receptors coded by homologous genes classified into four families: OR, TAAR, VR1 and VR2. Herein, we focus on the OR gene repertoire. While independent large contractions of the OR gene repertoire associated with ecological transitions have been found in mammals, little is known about the diversity of the OR gene repertoire and its evolution within teleost fishes, a group that includes more than 34,000 living species. We analyzed genomes of 163 species representing diversity in this large group. We found a large range of variation in the number of functional OR genes, from 15 in Syngnathus typhle and Mola mola, to 429 in Mastacembelus armatus. The number of OR genes was higher in species with an extensively folded olfactory epithelium, that is, for example, when a multi-lamellar rosette was present in the olfactory organ. Moreover, the number of lamellae was correlated with the richness of the OR gene repertoire. While a slow and balanced birth-and-death process generally drives evolution of the OR gene repertoire, we inferred several episodes of high rates of gene loss, sometimes followed by large gains in the number of OR genes. These gains coincide with morphological changes of the olfactory organ and suggest a strong functional association between changes in the morphology and the evolution of the OR gene repertoire.

evolutionary biology↗