Avian olfactory receptor gene repertoires: evidence for a well-developed sense of smell in birds?

Silke S Steiger,Mihai Valcu,Andrew E Fidler,Bart Kempenaers

doi:10.1098/rspb.2008.0607

Abstract

Among vertebrates, the sense of smell is mediated by olfactory receptors (ORs) expressed in sensory neurons within the olfactory epithelium. Comparative genomic studies suggest that the olfactory acuity of mammalian species correlates positively with both the total number and the proportion of functional OR genes encoded in their genomes. In contrast to mammals, avian olfaction is poorly understood, with birds widely regarded as relying primarily on visual and auditory inputs. Here, we show that in nine bird species from seven orders (blue tit, Cyanistes caeruleus; black coucal, Centropus grillii; brown kiwi, Apteryx australis; canary, Serinus canaria; galah, Eolophus roseicapillus; red jungle fowl, Gallus gallus; kakapo, Strigops habroptilus; mallard, Anas platyrhynchos; snow petrel, Pagodroma nivea), the majority of amplified OR sequences are predicted to be from potentially functional genes. This finding is somewhat surprising as one previous report suggested that the majority of OR genes in an avian (red jungle fowl) genomic sequence are non-functional pseudogenes. We also show that it is not the estimated proportion of potentially functional OR genes, but rather the estimated total number of OR genes that correlates positively with relative olfactory bulb size, an anatomical correlate of olfactory capability. We further demonstrate that all the nine bird genomes examined encode OR genes belonging to a large gene clade, termed γ-c, the expansion of which appears to be a shared characteristic of class Aves. In summary, our findings suggest that olfaction in birds may be a more important sense than generally believed.

Highlights

Olfactory receptors (ORs) expressed in sensory neurons within the olfactory epithelium constitute the molecular basis of the sense of smell among vertebrates (Buck & Axel 1991; Gaillard et al 2003)
We further investigated whether either the proportion of potentially functional olfactory receptors (ORs) genes or the estimated total number of OR genes correlates with the olfactory bulb ratio (OBR), a possible anatomical correlate of olfactory capability (Edinger 1908)
(b) Comparison of data based on degenerate PCR and genome search Of the 46 G. gallus sequences that we amplified using the degenerate PCR method, 18 were identical to the OR genes identified from the G. gallus genome search (BUILD v. 2.1, May 2006 release)

Summary

INTRODUCTION

Olfactory receptors (ORs) expressed in sensory neurons within the olfactory epithelium constitute the molecular basis of the sense of smell among vertebrates (Buck & Axel 1991; Gaillard et al 2003). Amplified avian partial OR-coding sequences were classified as being either non-g-c or g-c on the basis of sequence homologies between their corresponding predicted proteins and 78 potentially functional red jungle fowl (G. gallus) OR sequences of established classification ( Niimura & Nei 2005). 3. RESULTS (a) Proportion of potentially functional OR genes We amplified 46 distinct partial OR-coding sequences from red jungle fowl (G. gallus, order Galliformes) genomic DNA (table 1; table S1, electronic supplementary material). The large majority (95.7%) of the partial OR-coding sequences was predicted to be amplified from potentially functional OR genes To determine whether this high potentially functional/non-functional ratio is a general characteristic of bird genomes, we amplified between 26 and 68 (meanG s.e.m. 53.5G4.2) partial OR-coding sequences from a further eight species representing six additional avian orders (table 1; table S1, electronic supplementary material). Common name canary galah blue tit red jungle fowl mallard black coucal kakapo brown kiwi snow petrel scientific name order

Pagodroma nivea

Findings

DISCUSSION