Evolutionary Patterns and Selective Pressures of Odorant/Pheromone Receptor Gene Families in Teleost Fishes

Yasuyuki Hashiguchi,Yoshimi Furuta,Mutsumi Nishida,Alan Christoffels

doi:10.1371/journal.pone.0004083

Yasuyuki Hashiguchi, Yoshimi Furuta + Show 2 more

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https://doi.org/10.1371/journal.pone.0004083

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Abstract

BackgroundTeleost fishes do not have a vomeronasal organ (VNO), and their vomeronasal receptors (V1Rs, V2Rs) are expressed in the main olfactory epithelium (MOE), as are odorant receptors (ORs) and trace amine-associated receptors (TAARs). In this study, to obtain insights into the functional distinction among the four chemosensory receptor families in teleost fishes, their evolutionary patterns were examined in zebrafish, medaka, stickleback, fugu, and spotted green pufferfish.Methodology/Principal FindingsPhylogenetic analysis revealed that many lineage-specific gene gains and losses occurred in the teleost fish TAARs, whereas only a few gene gains and losses have taken place in the teleost fish vomeronasal receptors. In addition, synonymous and nonsynonymous nucleotide substitution rate ratios (KA/KS) in TAARs tended to be higher than those in ORs and V2Rs.Conclusions/SignificanceFrequent gene gains/losses and high KA/KS in teleost TAARs suggest that receptors in this family are used for detecting some species-specific chemicals such as pheromones. Conversely, conserved repertoires of V1R and V2R families in teleost fishes may imply that receptors in these families perceive common odorants for teleosts, such as amino acids. Teleost ORs showed intermediate evolutionary pattern between TAARs and vomeronasal receptors. Many teleost ORs seem to be used for common odorants, but some ORs may have evolved to recognize lineage-specific odors.

Highlights

Olfaction is a sense for recognizing chemicals in the external environment
Many species-specific clades were observed in teleost odorant receptors (ORs) and trace amine-associated receptors (TAARs)
To quantify the differences in phylogenetic patterns among the four evolutionary distinct chemosensory receptor families, the proportion of ‘‘species-specific’’ genes was estimated for each chemosensory receptor family in each species

Summary

Introduction

Olfaction is a sense for recognizing chemicals in the external environment. In many animals, olfaction is essential for various activities such as foraging, migration, and reproduction. Most terrestrial vertebrates have two distinct chemosensory organs, the main olfactory epithelium (MOE) and the vomeronasal organ (VNO). In the MOE, main odorant receptors (ORs) and trace amine-associated receptors (TAARs) are expressed, whereas in the VNO, vomeronasal receptors type 1 (V1Rs) and type 2 (V2Rs) are expressed [reviewed in 3]. This implies that in terrestrial vertebrates, ORs and TAARs are mainly used to recognize ‘‘ordinary’’ odorants, whereas V1Rs and V2Rs are used to recognize pheromones. Teleost fishes do not have a vomeronasal organ (VNO), and their vomeronasal receptors (V1Rs, V2Rs) are expressed in the main olfactory epithelium (MOE), as are odorant receptors (ORs) and trace amine-associated receptors (TAARs). To obtain insights into the functional distinction among the four chemosensory receptor families in teleost fishes, their evolutionary patterns were examined in zebrafish, medaka, stickleback, fugu, and spotted green pufferfish

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