Evolution of the Vomeronasal System Viewed through System-Specific Genes.

Abstract

Using three genes specific to the vomeronasal system (VNS), I addressed three questions about the evolution of this vertebrate sensory system that were previously unanswerable with only morphological data. (1) I investigated how the V1R vomeronasal receptor repertoire evolves in mammals. (2) I investigated how the patterns of evolution in VNS receptors compare to those of the main olfactory system (MOS). (3) I investigated when the VNS originated in vertebrate evolution. For the first question, I focused on three particular aspects of mammalian V1R evolution. First, I investigated how species-specificity evolves between two closely related mammals, mouse and rat, revealing that a gene-sorting birth and death model of evolution results in many species-specific duplication and loss of V1Rs and very few orthologous mouse-rat V1R pairs. Second, I investigated V1R repertoire size variation among five orders of mammals. Dramatic variation was observed with functional repertoire size varying over 20 times between dog and mouse. This study showed a correlation between VNS morphological complexity and V1R repertoire size. Finally, I examined V1R evolution in the platypus and found that it has the largest V1R repertoire thus far identified in vertebrates. These studies revealed independent expansions in V1Rs in all three mammalian lineages. To address my second question, I compared the proportion of genes resulting from lineage-specific gene gain or loss events for nasal chemoreceptors from both vertebrate olfactory systems. With this quantitative and functional comparative study, I revealed that a significantly higher proportion of VNS receptors evolved via lineage-specific events than did MOS receptors. The evolutionary patterns observed are consistent with the differential tuning hypothesis with main olfactory receptors being broadly tuned generalists and the VNS receptors being narrowly tuned specialists. Finally, to address my third question, I investigated the phylogenetic distribution of the VNS genetic components in early diverging lineages and determined that the VNS originated in the common ancestor of vertebrates. My work highlights the utility of system-specific genes and comparative genomics in understanding the evolution of a physiological system, and presents a much richer evolutionary history of the VNS than was thought to exist by morphological data alone.