Abstract

Olfactory receptors (ORs), encoded by the largest vertebrate multigene family, enable the detection of thousands of unique odorants in the environment and consequently play a critical role in species survival. Here, we advance our knowledge of OR gene evolution in procellariiform seabirds, an avian group which relies on the sense of olfaction for critical ecological functions. We built a cosmid library of Cory’s Shearwater (Calonectris borealis) genomic DNA, a model species for the study of olfaction-based navigation, and sequence OR gene-positive cosmid clones with a combination of sequencing technologies. We identified 220 OR open reading frames, 20 of which are full length, intact OR genes, and found a large ratio of partial and pseudogenes to intact OR genes (2:1), suggestive of a dynamic mode of evolution. Phylogenetic analyses revealed that while a few genes cluster with those of other sauropsid species in a γ (gamma) clade that predates the divergence of different avian lineages, most genes belong to an avian-specific γ-c clade, within which sequences cluster by species, suggesting frequent duplication and/or gene conversion events. We identified evidence of positive selection on full length γ-c clade genes. These patterns are consistent with a key role of adaptation in the functional diversification of olfactory receptor genes in a bird lineage that relies extensively on olfaction.

Highlights

  • Olfactory receptors (ORs), encoded by the largest vertebrate multigene family, enable the detection of thousands of unique odorants in the environment and play a critical role in species survival

  • We advance our knowledge of OR gene evolution in procellariiform seabirds, an avian group which relies on the sense of olfaction for critical ecological functions

  • Phylogenetic analyses revealed that while a few genes cluster with those of other sauropsid species in a γ clade that predates the divergence of different avian lineages, most genes belong to an avian-specific γ-c clade, within which sequences cluster by species, suggesting frequent duplication and/or gene conversion events

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Summary

Introduction

Olfactory receptors (ORs), encoded by the largest vertebrate multigene family, enable the detection of thousands of unique odorants in the environment and play a critical role in species survival. We identified evidence of positive selection on full length γ-c clade genes These patterns are consistent with a key role of adaptation in the functional diversification of olfactory receptor genes in a bird lineage that relies extensively on olfaction. Odour perception begins with the binding of odorant molecules to G protein-coupled receptors (GPCRs) primarily expressed in the nasal olfactory epithelium[3] These receptors, encoded by a complex multi-gene family containing large numbers of olfactory receptor (OR) genes[4], allow discrimination of a vast array of unique odorants. The striking variation in OR diversity patterns has been related to sensory trade-offs and lineage-specific ecological adaptation to new niches[5,6,10,12,18,19,20,21]. Based on patterns of variation and computational modeling in model organisms, the putative ligand binding sites are mainly located between the third and seventh transmembrane (TM) helical domains[22,23]

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