Lamprey possess both V1R and V2R olfactory receptors, but only V1Rs are expressed in olfactory sensory neurons

The sense of smell employs some of the largest gene families in the genome to detect and distinguish a multitude of different odors. Within vertebrates, 4 major olfactory receptor families have been described; of which, only 3 (OR, TAAR-like, and V1R) were found already in lamprey, a jawless vertebrate. The forth family (V2R) was believed to have originated later, in jawed vertebrates. Here we have delineated the entire vomeronasal receptor repertoire in 3 lamprey species. We report the presence of 6 v1r and 2 v2r genes in Lethenteron camtschaticum, arctic lamprey, and Lampetra fluviatilis, river lamprey (6 and 1, respectively, in sea lamprey, Petromyzon marinus). Three v1r genes but no v2r genes were found to be expressed in olfactory sensory neurons in the characteristic sparse expression pattern. Our results show the olfactory function of some V1Rs already in lamprey and, unexpectedly, an early origin of the V2R family in the shared ancestor of jawed and jawless vertebrates. However, lamprey v2r genes appear not to have acquired an olfactory function yet, thus dissociating the evolutionary origin of the family from the onset of a function as olfactory receptor.

Automated summary

The sense of smell relies on large gene families to detect and differentiate various odors. Four major olfactory receptor families have been discovered, with only three already present in lamprey, a jawless vertebrate. However, a fourth family was believed to have originated in jawed vertebrates. This study examined the complete vomeronasal receptor repertoire in three lamprey species and found evidence of v1r and v2r genes, indicating an early origin of the V2R family in the shared ancestor of jawed and jawless vertebrates. Despite the presence of v2r genes, lampreys have not yet acquired an olfactory function for this family, suggesting a disconnect between the evolutionary origin and functional onset of the V2R family as olfactory receptors.