MBE Advance Access published online on May 5, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn107
Research Article |
Distinct evolutionary patterns between chemoreceptors of two vertebrate olfactory systems and the differential tuning hypothesis
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA
* Correspondence to: Jianzhi Zhang, Department of Ecology and Evolutionary Biology, University of Michigan, 1075 Natural Science Building, 830 North University Avenue, Ann Arbor, MI 48109, Phone: 734-763-0527, Fax: 734-763-0544, Email: jianzhi{at}umich.edu
Received for publication February 5, 2008. Revision received April 10, 2008. Revision received April 27, 2008. Accepted for publication April 29, 2008.
Most tetrapod vertebrates have two olfactory systems, the main olfactory system (MOS) and the vomeronasal system (VNS). According to the dual olfactory hypothesis, the MOS detects environmental odorants while the VNS recognizes intraspecific pheromonal cues. However, this strict functional distinction has been blurred by recent reports that both systems can perceive both types of signals. Studies of a limited number of receptors suggest that MOS receptors are broadly tuned generalists while VNS receptors are narrowly tuned specialists. However, whether this distinction applies to all MOS and VNS receptors remains unknown. The differential tuning hypothesis predicts that generalist MOS receptors detect an overlapping set of ligands and thus are more likely to be conserved over evolutionary time than specialist VNS receptors, which would evolve in a more lineage-specific manner. Here we test this prediction for all olfactory chemoreceptors by examining the evolutionary patterns of MOS-expressed odorant receptors (ORs) and trace amine associated receptors (TAARs) and VNS-expressed vomeronasal type 1 receptors (V1Rs) and type 2 receptors (V2Rs) in seven tetrapods (mouse, rat, dog, opossum, platypus, chicken, and frog). The phylogenies of V1Rs and V2Rs show abundant lineage-specific gene gains/losses and virtually no one-to-one orthologs between species. Opposite patterns are found for ORs and TAARs. Analysis of functional data and ligand-binding sites of ORs confirms that paralogous chemoreceptors are more likely than orthologs to have different ligands and that functional divergence between paralogous chemoreceptors is established relatively quickly following gene duplication. Together, these results strongly suggest that the functional profile of the VNS chemoreceptor repertoire evolves much faster than that of the MOS chemoreceptor repertoire and that the differential tuning hypothesis applies to the majority, if not all, of MOS and VNS receptors.
Key Words: V1R • V2R • OR • TAAR • vomeronasal • olfactory