Abstract
In mammals, social and sexual behaviours are largely mediated by the vomeronasal system (VNS). The accessory olfactory bulb (AOB) is the first synaptic locus of the VNS and ranges from very large in Caviomorph rodents, small in carnivores and ungulates, to its complete absence in apes, elephants, most bats and aquatic species. Two pathways have been described in the VNS of mammals. In mice, vomeronasal neurons expressing Gαi2 protein project to the rostral portion of the AOB and respond mostly to small volatile molecules, whereas neurons expressing Gαo project to the caudal AOB and respond mostly to large non-volatile molecules. However, the Gαo-expressing pathway is absent in several species (horses, dogs, musk shrews, goats and marmosets) but no hypotheses have been proposed to date to explain the loss of that pathway. We noted that the species that lost the Gαo pathway belong to Laurasiatheria and Primates lineages, both clades with ubiquitous sexual dimorphisms across species. To assess whether similar events of Gαo pathway loss could have occurred convergently in dimorphic species we studied G-protein expression in the AOB of two species that independently evolved sexually dimorphic traits: the California ground squirrel Spermophilus beecheyi (Rodentia; Sciurognathi) and the cape hyrax Procavia capensis (Afrotheria; Hyracoidea). We found that both species show uniform expression of Gαi2-protein throughout AOB glomeruli, while Gαo expression is restricted to main olfactory glomeruli only. Our results suggest that the degeneration of the Gαo-expressing vomeronasal pathway has occurred independently at least four times in Eutheria, possibly related to the emergence of sexual dimorphisms and the ability of detecting the gender of conspecifics at distance.
Highlights
The mammalian vomeronasal system (VNS) mediates in the perception of pheromones and the orchestration of bodily responses related to social and sexual interactions [1]
Neurons located near the apex of the vomeronasal organ (VNO) lumen express pheromone receptors of the V1R family, which are coupled to Gai2-protein, and send projections to glomeruli located in the rostral half of the accessory olfactory bulb (AOB)
We studied Gai2 and Gao expression in AOB glomeruli of the California ground squirrel Spermophilus beecheyi and the cape hyrax Procavia capensis
Summary
The mammalian vomeronasal system (VNS) mediates in the perception of pheromones and the orchestration of bodily responses related to social and sexual interactions [1]. The accessory olfactory bulb (AOB) is the first synaptic locus of the VNS and receives afferents from sensory neurons of the vomeronasal organ (VNO). Two anatomical and functionally distinct pathways have been described in the mammalian VNS [2,3,10,11,12,13,14]. Neurons located near the apex of the VNO lumen express pheromone receptors of the V1R family, which are coupled to Gai2-protein, and send projections to glomeruli located in the rostral half of the AOB. Neurons at the base of the VNO express V2R receptors coupled to Gao-protein and send projections to glomeruli of the caudal AOB [10,12,15,16, 17,18,19,20]. Each pathway has a distinct sensorial specificity: while V1R receptors have a small extracellular ligand-binding Ndomain [17,18] and show high affinity for small and volatile molecules [21,22], V2R receptors have a large N-domain [17,18,19] and show high affinity for large non-volatile molecules, such as urinary proteins and exocrine gland-secreted peptides [23,24,25,26]
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