Type 1 vomeronasal receptors expressed in the olfactory organs of two African lungfish, Protopterus annectens and Protopterus amphibius

Abstract

Lungfish are the fish related most closely to tetrapods. The olfactory organ of lungfish contains two distinct sensory epithelia: the lamellar olfactory epithelium (OE) and the recess epithelium (RecE). Based on their ultrastructural and histological characteristics, the lamellar OE and the RecE are considered to correspond respectively to the teleost OE and a primitive vomeronasal organ (VNO). In tetrapods, the OE and VNO have been shown to express different families of olfactory receptors; for example, in mammals, the OE expresses odorant receptors and trace amine‐associated receptors, while the VNO expresses type 1 (V1Rs) and type 2 (V2Rs) vomeronasal receptors. In the present study, we examined the expression of V1Rs in the olfactory organs of two African lungfish, Protopterus annectens and Protopterus amphibius. RNA sequencing and phylogenetic analyses identified 29 V1R genes in P. annectens and 50 V1R genes in P. amphibius. Most V1Rs identified in these lungfish were classified as the tetrapod‐type V1Rs initially found in tetrapods and distinct from fish‐type V1Rs. In teleost, which all lack a VNO, all olfactory receptors are expressed in the OE, while in Xenopus V1Rs are expressed exclusively in the OE, and not in the VNO. In situ hybridization analysis indicated that lungfish V1Rs were expressed mainly in the lamellar OE and rarely in the RecE. These results imply that V1R expression in lungfish represents an intermediate step toward the complete segregation of V1R expression between the OE and VNO, reflecting the phylogenetic position of lungfish between teleosts and amphibians.

Pheromone Sensing in Mammals: A Review of the Vomeronasal System

“…Evolutionarily, the vomeronasal system has been linked to the transition of vertebrates to terrestrial environments; however, recent evidence suggests that a precursor VNS exists in teleost fish and its evolutionary origin predates the divergence between teleosts and tetrapods [10,198]. Added to this is the unique case of several species of lungfish that have a vomeronasal system homologous to mammals, showcasing a defined vomeronasal organ and an accessory olfactory bulb [199][200][201][202]. Hence, the significance of chemical communication has been a constant throughout the evolutionary history of vertebrates, resulting in significant morphofunctional variations among the chemosensory systems of different species.…”

Pheromone Sensing in Mammals: A Review on the Vomeronasal System

“…Evolutionarily, the vomeronasal system has been linked to the transition of vertebrates to terrestrial environments; however, recent evidence suggests that a precursor SVN exists in teleost fish and its evolutionary origin predates the divergence between teleosts and tetrapods [10,198]. Added to this is the unique case of several species of lungfish that have a vomeronasal system homologous to mammals, showcasing a defined vomeronasal organ and an accessory olfactory bulb [199][200][201][202]. Hence, the significance of chemical communication has been a constant throughout the evolutionary history of vertebrates, resulting in significant morphofunctional variations among the chemosensory systems of different species.…”