Origin and evolution of the vertebrate vomeronasal system viewed through system‐specific genes

Abstract

Tetrapods have two distinct nasal chemosensory systems, the main olfactory system and the vomeronasal system (VNS). Defined by certain morphological components, the main olfactory system is present in all groups of vertebrates, while the VNS is found only in tetrapods. Previous attempts to identify a VNS precursor in teleost fish were limited by functional and morphological characters that could not clearly distinguish between homologous and analogous systems. In the past decade, several genes that specifically function in the VNS have been discovered. Here we first describe recent evolutionary studies of mammalian VNS-specific genes. We then review evidence showing the presence and tissue-specific expression of the VNS-specific genes in teleosts, as well as co-expression patterns of these genes in specific regions of the teleost olfactory epithelium. We propose that a VNS precursor exists in teleosts and that its evolutionary origin predated the separation between teleosts and tetrapods.

Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land

“…The frog expansions of both vomeronasal receptor gene families may be related to the origin of the VNO. Although teleosts have V1R and V2R genes, they do not have VNOs (Grus and Zhang 2006). Instead, teleost V1R and V2R genes are expressed in the microvillar sensory neurons in the olfactory epithelium, which has been suggested to be homologous to tetrapod vomeronasal sensory neurons (Grus and Zhang 2006).…”

“…It is likely that the pseudogenization of various genes involved in the chicken vomeronasal transduction pathway took place so long ago that even V1R pseudogenes are unidentifiable from the chicken genome. Similarly, the gene encoding TRPC2, an ion channel indispensable for vomeronasal transduction, is also absent in the chicken genome (Grus and Zhang 2006). In parallel to the ancient loss of the VNO in birds, an independent loss in catarrhine primates (humans, apes, and Old World monkeys) occurred about 23 million years ago (Zhang and Webb 2003).…”

“…Previous analyses identified 187 intact V1R genes and 61 intact V2R genes in the mouse genome. Most, if not all V1R and V2R genes, are expressed in the VNO of terrestrial vertebrates (Dulac and Torello 2003) or the MOE of teleost fishes (Cao et al 1998;Pfister and Rodriguez 2005), as fishes do not have the VNO (Grus and Zhang 2006). It is believed that each vomeronasal sensory neuron expresses only one allele of either a V1R or a V2R gene (Dulac and Torello 2003).…”

Extraordinary Diversity of Chemosensory Receptor Gene Repertoires Among Vertebrates

“…Thus, the nomenclature of the fish chemosensory receptors that are homologous to mammalian vomeronasal receptors has been confusing. On the basis of sequence homology, some authors termed them "V1R-like" and "V2R-like" genes Nishida 2005 , 2006 ;Pfister and Rodriguez 2005 ;Pfister et al 2007) , while some authors separately designated them as "olfactory receptor A family GPCR" and "olfactory receptor C family GPCR" by considering their expression pattern and phylogenetic position in the GPCR family (Alioto and Ngai 2006 ;Saraiva and Korsching 2007 (Grus and Zhang 2006) . Third, the latter nomenclature is also confusing and undistinguishable from that for other chemosensory receptors expressed in the MOE.…”

“…Similarly, the lack of the TRPC2 gene and V1R and V2R genes is observed in chicken, reflecting the ancient loss of the VNO in birds. Conversely, the TRPC2 open reading frame is maintained in all vertebrates known to have functional vomeronasal receptors (Grus and Zhang 2006) .…”