The strange case of the chondrichthyan olfactory system

The main olfactory system has been identified in all the classes of vertebrates, while the vomeronasal system is lacking in some groups, such as birds and primates, which presumably have lost it. Chondrichthyes are one of seven vertebrate classes. The peripheral olfactory organs of these fishes are large olfactory rosettes, with a huge sensory surface, which does not bear sensory cilia, a unique condition in all studied vertebrates (Ferrando and Gallus, 2013). Only the genome of one species, elephant shark Callorhinchus milii, has been sequenced to date and only 3 genes for olfactory receptor (ORs) and 2 genes for trace amine-associated receptors (TAARs) were found (Venkatesh et al., 2014). However, 1 gene belonging to the vomeronasal receptor family of type 1 (V1Rs) and 32 genes of type 2 (V2Rs) have been identified in C. milii . We applied immunohistochemical methods on the peripheral olfactory organ of different Chondrichthyes in order to detect the presence and distribution of G protein alpha subunits, usually coupled to ORs and V2Rs. The immunohistochemical detection of G protein α subunits in the olfactory organ of the elasmobranchScyliorhinus canicula, Etmopterus spinax, Raja clavata, Raja asterias, Torpedo marmorataand the holocephalan Chimaera monstrosa, did not reveal the presence of Gαolf, highlighting the presence of Gαo and/or Gαi in virtually all sensory neurons. Moreover, as the gene for Gαolf is present in the C. miliigenome, we investigate the expression of mRNA for Gαolf in the olfactory rosette of C. milii , C. monstrosa and S. canicula , and we found it is not expressed. From our data and from the literature, we can suggest that Chondrichthyes presents a very particular olfactory system, compared to that of all the other vertebrates, showing almost exclusively vomeronasal features. Further investigations could lead to interesting acquisitions on the biology of these fishes and on the evolution of chemoreception in vertebrates.