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Steiger, Silke (2008): Evolution of avian olfaction. Dissertation, LMU München: Faculty of Biology
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Abstract

The sense of smell enables animals to e.g. locate food, to navigate or to avoid predators. In vertebrates, odorants are detected by olfactory receptors (ORs) that are expressed in the olfactory epithelium on olfactory sensory neurons. In this study, I investigated OR gene repertoires in both closely and distantly related bird species. Using polymerase chain reaction (PCR) with degenerate primers designed to amplify OR genes, I showed that the majority of OR genes sequenced (~ 84%) were potentially functional in nine bird species from seven different orders. A nonparametric statistical technique was used to estimate the total number of OR genes in avian genomes. The total number of OR genes was surprisingly large and varied up to six fold between species (range: 106 – 667 OR genes). The total number of OR genes but not the proportion of potentially functional OR genes was positively correlated with the relative size of the olfactory bulb, which is considered an anatomical correlate of olfactory capability. A Southern Blot approach in combination with a PCR based approach revealed that two nocturnal bird species that heavily rely on olfactory cues, have evolved a larger OR gene repertoire than their diurnal, closest living relatives. Thus, it is likely that ecological niche adaptations (e.g. adaptations related to daily activity patterns) have shaped avian OR gene repertoires. Phylogenetic trees derived from predicted OR protein sequences revealed that a large, expanded OR gene clade, termed group-γ-c, is present in all bird genomes examined in this study. This clade seems to be a shared characteristic of all bird genomes. Further, I showed that positive selection has driven the molecular evolution of avian group-γ-c OR genes. Positively selected sites encoded residues within transmembrane regions that most likely interact with odour molecules and thus might influence OR receptor functioning. Interestingly, OR gene transcripts have been detected in testis and sperm of both mammals and fish, suggesting that OR genes are also involved in sperm-egg communication. Using reverse transcription (RT)-PCR with degenerate primers specific for OR genes, and subsequent cloning, I showed that several OR gene transcripts are present in chicken (Gallus gallus domesticus) testes and that they belong to the class-γ OR gene clade. Finally, a database search in the red jungle fowl (Gallus gallus) genome revealed that trace amine-associated receptors (TAARs) - a second family of chemosensory receptors primarily expressed in the olfactory epithelium that detect amine-based odour cues - are also encoded in avian genomes. The findings in this thesis contribute to our understanding of the evolution of avian OR genes. The estimated OR gene repertoire sizes, and the proportion of presumably functional OR genes, strongly suggest that avian olfactory ability is well developed and much more important than previously thought.