Abstract
Olfactory receptor families have arisen independently several times during evolution. The origin of taar genes, one of the four major vertebrate olfactory receptor families, is disputed. We performed a phylogenetic analysis making use of 96 recently available genomes, and report that olfactory functionality has arisen twice independently within the TAAR family, once in jawed and once in jawless fish. In lamprey, an ancestral gene expanded to generate a large family of olfactory receptors, while the sister gene in jawed vertebrates did not expand and is not expressed in olfactory sensory neurons. Both clades do not exhibit the defining TAAR motif, and we suggest naming them taar-like receptors (tarl). We have identified the evolutionary origin of both taar and tarl genes in a duplication of the serotonergic receptor 4 that occurred in the most recent common ancestor of vertebrates. We infer two ancestral genes in bony fish (TAAR12, TAAR13) which gave rise to the complete repertoire of mammalian olfactory taar genes and to class II of the taar repertoire of teleost fish. We follow their evolution in seventy-one bony fish genomes and report a high evolutionary dynamic, with many late gene birth events and both early and late gene death events.
Highlights
Olfactory receptor families have arisen independently several times during evolution
There exists some controversy about the evolutionary origin of the Trace amine-associated receptors (TAARs) family, which variously has been described to originate in jawed vertebrates, vertebrates, and even non-vertebrate chordates[4,5,8]
TAAR12 was found to be absent in neoteleosts, consistent with earlier hypotheses[5], but TAAR13 was detected in a minority of neoteleost species, suggesting several independent gene death events
Summary
Olfactory receptor families have arisen independently several times during evolution. An initial phylogenetic analysis showed the presence of the family in teleost fish[2] and subsequently their function as olfactory receptors was revealed[3,4] Another phylogenetic study found the TAAR repertoire sizes in five teleost species to be several-fold larger than those of tetrapods and suggested a subdivision of the TAAR family in three classes[5]. To identify the founding gene which gave rise to the TAAR family and to understand the evolution of class II taar genes, we have performed a phylogenetic analysis in 96 deuterostome genomes These species cover a wide evolutionary range, from the sister group of chordates to non-vertebrate chordates to jawless vertebrates to cartilaginous fish to a broad range of bony fish species representing many of the major phylogenetic subdivisions in this most numerous clade of all vertebrates. TAAR12 was found to be absent in neoteleosts, consistent with earlier hypotheses[5], but TAAR13 was detected in a minority of neoteleost species, suggesting several independent gene death events
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