The sea lamprey has a primordial accessory olfactory system.

BACKGROUND: A dual olfactory system, represented by two anatomically distinct but spatially proximate chemosensory epithelia that project to separate areas of the forebrain, is known in several classes of tetrapods. Lungfish are the earliest evolving vertebrates known to have this dual system, comprising a main olfactory and a vomeronasal system (VNO). Lampreys, a group of jawless vertebrates, have a single nasal capsule containing two anatomically distinct epithelia, the main (MOE) and the accessory olfactory epithelia (AOE). We speculated that lamprey AOE projects to specific telencephalic regions as a precursor to the tetrapod vomeronasal system. RESULTS: To test this hypothesis, we characterized the neural circuits and molecular profiles of the accessory olfactory epithelium in the sea lamprey (Petromyzon marinus). Neural tract-tracing revealed direct and reciprocal connections with the dorsomedial telencephalic neuropil (DTN) which in turn projects directly to the dorsal pallium and the rostral hypothalamus. High-throughput sequencing demonstrated that the main and the accessory olfactory epithelia have virtually identical profiles of expressed genes. Real time quantitative PCR confirmed expression of representatives of all 3 chemoreceptor gene families identified in the sea lamprey genome. CONCLUSION: Anatomical and molecular evidence shows that the sea lamprey has a primordial accessory olfactory system that may serve a chemosensory function.

The sea lamprey Petromyzon marinus genome reveals the early origin of several chemosensory receptor families in the vertebrate lineage.

BACKGROUND: In gnathostomes, chemosensory receptors (CR) expressed in olfactory epithelia are encoded by evolutionarily dynamic gene families encoding odorant receptors (OR), trace amine-associated receptors (TAAR), V1Rs and V2Rs. A limited number of OR-like sequences have been found in invertebrate chordate genomes. Whether these gene families arose in basal or advanced vertebrates has not been resolved because these families have not been examined systematically in agnathan genomes. RESULTS: Petromyzon is the only extant jawless vertebrate whose genome has been sequenced. Known to be exquisitely sensitive to several classes of odorants, lampreys detect fewer amino acids and steroids than teleosts. This reduced number of detectable odorants is indicative of reduced numbers of CR gene families or a reduced number of genes within CR families, or both, in the sea lamprey. In the lamprey genome we identified a repertoire of 59 intact single-exon CR genes, including 27 OR, 28 TAAR, and four V1R-like genes. These three CR families were expressed in the olfactory organ of both parasitic and adult life stages. CONCLUSION: An extensive search in the lamprey genome failed to identify potential orthologs or pseudogenes of the multi-exon V2R family that is greatly expanded in teleost genomes, but did find intact calcium-sensing receptors (CASR) and intact metabotropic glutamate receptors (MGR). We conclude that OR and V1R arose in chordates after the cephalochordate-urochordate split, but before the diversification of jawed and jawless vertebrates. The advent and diversification of V2R genes from glutamate receptor-family G protein-coupled receptors, most likely the CASR, occurred after the agnathan-gnathostome divergence.