Abstract
The olfactory system meets niche- and species-specific demands by an accelerated evolution of its odorant receptor repertoires. In this review, we describe evolutionary processes that have shaped olfactory and vomeronasal receptor gene families in vertebrate genomes. We emphasize three important periods in the evolution of the olfactory system evident by comparative genomics: the adaptation to land in amphibian ancestors, the decline of olfaction in primates, and the delineation of putative pheromone receptors concurrent with rodent speciation. The rapid evolution of odorant receptor genes, the sheer size of the repertoire, as well as their wide distribution in the genome, presents a developmental challenge: how are these ever-changing odorant receptor repertoires coordinated within the olfactory system? A central organizing principle in olfaction is the specialization of sensory neurons resulting from each sensory neuron expressing only ~one odorant receptor allele. In this review, we also discuss this mutually exclusive expression of odorant receptor genes. We have considered several models to account for co-regulation of odorant receptor repertoires, as well as discussed a new hypothesis that invokes important epigenetic properties of the system.
Highlights
Animals depend on chemosensory systems to investigate their environments and to communicate social and reproductive status
We describe the regulation of the expression of these odorant receptor repertoires during development, since, as we will discuss, olfactory receptor (OR) co-regulation is the basis for an organizing principle that permits the brain to interpret smells
OR and V1R genes are co-regulated such that each sensory neuron expresses only ~one of the large repertoire of these genes
Summary
Animals depend on chemosensory systems to investigate their environments and to communicate social and reproductive status. Cluster organization in the genome The large, diverse repertoire of mammalian odorant receptors is organized in clusters at various chromosomal locations in the genome (Fig. 4a) These clusters are arrays of closely related genes, reflecting an evolutionary history of recent tandem duplications. There is evidence of fixation of some ancestral functions, such as Class I ORs in mammals [19,84] or specific OR orthologs between mouse and human (e.g., [47,85,86]), this evolutionary history can be described as "volcanic" – frequent gene duplication, gene deletion, recombination, gene conversion, pseudogenization, and positive selection have shaped very different repertoires between and within species. Additional experiments will be required to clarify the role of the "H region", the molecular basis for stochastic properties of OR selection, and the importance, if any, of epigenetics in the monogenic and monoallelic expression of receptors in the olfactory and vomeronasal systems
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