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Abstract Lungfish are the most closely related fish to tetrapods. The olfactory organ of lungfish contains lamellae and abundant recesses at the base of lamellae. Based on the ultrastructural and histochemical characteristics, the lamellar olfactory epithelium (OE), covering the surface of lamellae, and the recess epithelium, contained in the recesses, are thought to correspond to the OE of teleosts and the vomeronasal organ (VNO) of tetrapods. With increasing body size, the recesses increase in number and distribution range in the olfactory organ. In tetrapods, the expression of olfactory receptors is different between the OE and VNO; for instance, the type 1 vomeronasal receptor (V1R) is expressed only in the OE in amphibians and mainly in the VNO in mammals. We recently reported that V1R-expressing cells are contained mainly in the lamellar OE but also rarely in the recess epithelium in the olfactory organ of lungfish of approximately 30 cm body length. However, it is unclear whether the distribution of V1R-expressing cells in the olfactory organ varies during development. In this study, we compared the expression of V1Rs in the olfactory organs between juveniles and adults of the African lungfish Protopterus aethiopicus and South American lungfish, Lepidosiren paradoxa. The density of V1R-expressing cells was higher in the lamellae than in the recesses in all specimens evaluated, and this pattern was more pronounced in juveniles than adults. In addition, the juveniles showed a higher density of V1R-expressing cells in the lamellae compared with the adults. Our results imply that differences in lifestyle between juveniles and adults are related to differences in the density of V1R-expressing cells in the lamellae of lungfish.

Abstract The vomeronasal type 2 receptor (V2R, also called OlfC) multigene family is found in a broad range of jawed vertebrates from cartilaginous fish to tetrapods. V2Rs encode receptors for food-related amino acids in teleost fish, whereas for peptide pheromones in mammals. In addition, V2Rs of teleost fish are phylogenetically distinct from those of tetrapods, implying a drastic change in the V2R repertoire during terrestrial adaptation. To understand the process of diversification of V2Rs in vertebrates from “fish-type” to “tetrapod-type”, we conducted an exhaustive search for V2Rs in cartilaginous fish (chimeras, sharks, and skates) and basal ray-finned fish (reedfish, sterlet, and spotted gar), and compared them with those of teleost, coelacanth, and tetrapods. Phylogenetic and synteny analyses on 1897 V2Rs revealed that basal ray-finned fish possess unexpectedly higher number of V2Rs compared with cartilaginous fish, implying that V2R gene repertoires expanded in the common ancestor of Osteichthyes. Furthermore, reedfish and sterlet possessed various V2Rs that belonged to both “fish-type” and “tetrapod-type”, suggesting that the common ancestor of Osteichthyes possess “tetrapod-type” V2Rs although they inhabited underwater environments. Thus, the unexpected diversity of V2Rs in basal ray-finned fish may provide insight into how the olfaction of osteichthyan ancestors adapt from water to land.

Abstract Fish possess one olfactory organ called the olfactory epithelium (OE), by which various chemical substances are detected. On the other hand, tetrapods possess two independent olfactory organs called the main olfactory epithelium (MOE) and vomeronasal organ (VNO), each of which mainly detects general odorants and pheromones, respectively. Traditionally, the VNO, so-called concentrations of vomeronasal neurons, was believed to have originated in tetrapods. However, recent studies have identified a primordial VNO in lungfish, implying that the origin of the VNO was earlier than traditionally expected. In this study, we examined the presence/absence of the VNO in the olfactory organ of bichir (Polypterus senegalus), which is the most ancestral group of extant bony vertebrates. In particular, we conducted a transcriptomic evaluation of the accessory olfactory organ (AOO), which is anatomically separated from the main olfactory organ (MOO) in bichir. As a result, several landmark genes specific to the VNO and MOE in tetrapods were both expressed in the MOO and AOO, suggesting that these organs were not functionally distinct in terms of pheromone and odorant detection. Instead, differentially expressed gene (DEG) analysis showed that DEGs in AOO were enriched in genes for cilia movement, implying its additional and specific function in efficient water uptake into the nasal cavity other than chemosensing. This transcriptomic study provides novel insight into the long-standing question of AOO function in bichir and suggests that VNO originated in the lineage of lobe-finned fish during vertebrate evolution.