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

Abstract

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 ray-finned fishes is heterogeneous and presents a dynamic pattern of evolutionary expansions, simplifications, and reacquisitions.

Ancient and nonuniform loss of olfactory receptor expression renders the shark nose ade factovomeronasal organ

“…The V1R/ORA family of cartilaginous fish is small, similar to that of many teleosts (Saraiva and Korsching 2007; Zapilko and Korsching 2016), but see (Policarpo et al, 2022). All genes were examined for expression individually using in situ hybridisation.…”

“…Such a low number of olfactory receptors is otherwise only known for species having a highly degenerated olfactory system, e.g. toothed whales (Kishida et al 2015) and ocean sunfishes (Policarpo et al 2021, 2022). However, in contrast to these species, cartilaginous fishes have well developed olfactory organs with a large sensory surface.…”

Ancient and Nonuniform Loss of Olfactory Receptor Expression Renders the Shark Nose a De Facto Vomeronasal Organ

“…Olfactory receptor families not expressed in the olfactory organ (i.e., with nonolfactory function) are marked by red overlay; families with minor expression in OSNs are marked by yellow overlay. Gene numbers are taken from these studies: ( a ) Petromyzon marinus ( Niimura 2009) ; ( b ) Lethenteron camtschaticum ( Dieris et al 2021) (number refers to TARL, the sister group of TAAR, which are absent in lamprey); ( c and d ) L. camtschaticum ( Kowatschew and Korsching 2022) ; ( e and h ) C. milii (this study); (f and g) S. canicula (this study); ( i ) Loxodonta africana ( Niimura et al 2014) ; ( j ) Monodelphis domestica ( Grus et al 2007) ; ( k ) Ornithorhynchus anatinus ( Grus et al 2007) ; ( l ) Xenopus tropicalis ( Ji et al 2009) ; and ( m ) Erpetoichthys calabaricus ( Policarpo et al 2022) .…”

“…The V1R/ORA family of cartilaginous fish is small, similar to that of many teleosts ( Saraiva and Korsching 2007 ; Zapilko and Korsching 2016 ), but see Policarpo et al (2022) . All genes were examined for expression individually using in situ hybridization.…”

“…In most bony fishes, there are hundreds to thousands of olfactory receptor coding genes, but the genome of cartilaginous fishes codes only for ∼10–50 olfactory receptors. Such a low number of olfactory receptors is otherwise only known for species having a highly degenerated olfactory system, for example, toothed whales ( Kishida et al 2015 ) and ocean sunfishes ( Policarpo et al 2021 , 2022 ). However, in contrast to these species, cartilaginous fishes have well-developed olfactory organs with a large sensory surface.…”