Ray-finned fishes perceive their environment through a range of sensory modalities, including olfaction.

Background: Ray-finned fishes (Actinopterygii) perceive their environment through a range of sensory modalities, including olfaction. Anatomical diversity of the olfactory organ suggests that olfaction is differentially important among species. To explore this topic, we studied the evolutionary dynamics of the four main gene families (OR, TAAR, ORA/VR1 and OlfC/VR2) coding for olfactory receptors in 185 species of ray-finned fishes.

Results: 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, Polypteriformes, which have a unique and complex olfactory organ, have almost twice as many olfactory receptor genes as any other ray-finned fish.

Conclusions: We document 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 rayfinned fishes is heterogeneous and presents a dynamic pattern of evolutionary expansions, simplifications, and reacquisitions.

Coevolution of the olfactory organ and its receptor repertoire in ray-finned fishes. Maxime Policarpo, Katherine Bemis, Patrick Laurenti, Laurent Legendre, Jean-Christophe Sandoz, Sylvie Rétaux, Didier Casane.

Morpho-genomic space of olfaction in ray-finned fishes.
A Diversity of olfactory organ morphology. Syngnathus typhle, 283 mm TL, Mola mola, 1290 cm TL, Takifugu rubripes 290 mm TL, Danio rerio, 30 mm TL, Anguilla anguilla, 450 mm TL, Erpetoichthys calabaricus, 268 mm TL, Polypterus senegalus, 112 mm TL. Anterior to left.
B Correlation between number of olfactory lamellae and number of olfactory receptor genes; all fishes examined, ranging from microsmatic to macrosomatic, occurred in the blue region of the graph. Most evolutionary transitions in the olfactory organ, indicated by arrows, were simplifications (e.g., S. typhle, M. mola), but expansions (e.g., A. anguilla, E. calabaricus, and P. senegalus) and reacquisition (e.g., T. rubripes) also occurred.

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