Olfactory Receptor Subgenomes Linked with Broad Ecological Adaptations in Sauropsida.

Abstract

Olfactory receptors (ORs) govern a prime sensory function. Extant birds have distinct olfactory abilities, but the molecular mechanisms underlining diversification and specialization remain mostly unknown. We explored OR diversity in 48 phylogenetic and ecologically diverse birds and 2 reptiles (alligator and green sea turtle). OR subgenomes showed species- and lineage-specific variation related with ecological requirements. Overall 1,953 OR genes were identified in reptiles and 16,503 in birds. The two reptiles had larger OR gene repertoires (989 and 964 genes, respectively) than birds (182-688 genes). Overall, birds had more pseudogenes (7,855) than intact genes (1,944). The alligator had significantly more functional genes than sea turtle, likely because of distinct foraging habits. We found rapid species-specific expansion and positive selection in OR14 (detects hydrophobic compounds) in birds and in OR51 and OR52 (detect hydrophilic compounds) in sea turtle, suggestive of terrestrial and aquatic adaptations, respectively. Ecological partitioning among birds of prey, water birds, land birds, and vocal learners showed that diverse ecological factors determined olfactory ability and influenced corresponding olfactory-receptor subgenome. OR5/8/9 was expanded in predatory birds and alligator, suggesting adaptive specialization for carnivory. OR families 2/13, 51, and 52 were correlated with aquatic adaptations (water birds), OR families 6 and 10 were more pronounced in vocal-learning birds, whereas most specialized land birds had an expanded OR family 14. Olfactory bulb ratio (OBR) and OR gene repertoire were correlated. Birds that forage for prey (carnivores/piscivores) had relatively complex OBR and OR gene repertoires compared with modern birds, including passerines, perhaps due to highly developed cognitive capacities facilitating foraging innovations.

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Published Version (Please cite this version)

10.1093/molbev/msv155

Publication Info

Khan, Imran, Zhikai Yang, Emanuel Maldonado, Cai Li, Guojie Zhang, M Thomas P Gilbert, Erich D Jarvis, Stephen J O'Brien, et al. (2015). Olfactory Receptor Subgenomes Linked with Broad Ecological Adaptations in Sauropsida. Mol Biol Evol, 32(11). pp. 2832–2843. 10.1093/molbev/msv155 Retrieved from https://hdl.handle.net/10161/11139.

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Jarvis

Erich David Jarvis

Adjunct Professor in the Department of Neurobiology

Dr. Jarvis' laboratory studies the neurobiology of vocal communication. Emphasis is placed on the molecular pathways involved in the perception and production of learned vocalizations. They use an integrative approach that combines behavioral, anatomical, electrophysiological and molecular biological techniques. The main animal model used is songbirds, one of the few vertebrate groups that evolved the ability to learn vocalizations. The generality of the discoveries is tested in other vocal learning orders, such as parrots and hummingbirds, as well as non-vocal learners, such as pigeons and non-human primates. Some of the questions require performing behavior/molecular biology experiments in freely ranging animals, such as hummingbirds in tropical forest of Brazil. Recent results show that in songbirds, parrots and hummingbirds, perception and production of song are accompanied by anatomically distinct patterns of gene expression. All three groups were found to exhibit vocally-activated gene expression in exactly 7 forebrain nuclei that are very similar to each other. These structures for vocal learning and production are thought to have evolved independently within the past 70 million years, since they are absent from interrelated non-vocal learning orders. One structure, Area X of the basal ganglia's striatum in songbirds, shows large differential gene activation depending on the social context in which the bird sings. These differences may reflect a semantic content of song, perhaps similar to human language.

The overall goal of the research is to advance knowledge of the neural mechanisms for vocal learning and basic mechanisms of brain function. These goals are further achieved by combined collaborative efforts with the laboratories of Drs. Mooney and Nowicki at Duke University, who study respectively behavior and electrophysiological aspects of songbird vocal communication.


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