Shifts in type 2 vomeronasal receptor expression during postnatal development in the lungfish olfactory organ

Abstract

Many tetrapods possess two distinct olfactory organs: the olfactory epithelium (OE) and the vomeronasal organ (VNO). Fish have only the OE, but lungfish—the closest living relative of tetrapods among fish— possess a lamellar OE and a primitive VNO called a recess epithelium (RecE). Vomeronasal receptor type 2 (V2R) genes in lungfish can be classified into three categories: those expressed only in the lamellar OE, those expressed only in the RecE, and those expressed in both the lamellar OE and the RecE. In this study, we compared V2R expression patterns in Protopterus annectens of different body sizes to examine how expression changes with growth. V2Rs expressed exclusively in the lamellar OE in small individuals remained restricted to the lamellar OE in large individuals, and V2Rs expressed exclusively in the RecE in small individuals also remained RecE-specific in large individuals. In contrast, among the V2Rs expressed in both the lamellar OE and the RecE in small individuals, some maintained expression in both tissues, while others became restricted to the RecE in large individuals. Medium-sized individuals showed intermediate expression patterns between small and large specimens. These results suggest that a subset of V2Rs initially expressed in both the lamellar OE and the RecE lose expression in the lamellar OE as the individual matures, becoming restricted to the RecE, and that functional separation between the lamellar OE and the RecE is still incomplete in juveniles and becomes more distinct during growth. These findings might represent the developmental process of the bimodal olfactory system in vertebrates. In the common ancestors of lungfish and tetrapods, there might be no functional separation between the OE and VNO. However, it can be speculated that olfactory functions have partially separated between the OE (lamellar OE) and VNO (RecE) in extant lungfish, while they have completely separated between the OE and VNO in extant tetrapods which acquired more developed VNO.