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Mol Biol Evol. 2015 Nov;32(11):2832-43. doi: 10.1093/molbev/msv155. Epub 2015 Jul 28.

Olfactory Receptor Subgenomes Linked with Broad Ecological Adaptations in Sauropsida.

Author information

1
CIIMAR/CIMAR, Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Porto, Portugal Department of Biology, Faculty of Sciences, University of Porto, Porto, Portugal.
2
China National Genebank, BGI-Shenzhen, 518083, Shenzhen, Guangdong, China.
3
CIIMAR/CIMAR, Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Porto, Portugal.
4
China National Genebank, BGI-Shenzhen, 518083, Shenzhen, Guangdong, China Centre for Social Evolution, Department of Biology, Universitetsparken 15, University of Copenhagen, DK-2100 Copenhagen, Denmark.
5
Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark.
6
Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center.
7
Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, St. Petersburg, Russia Oceanographic Center, Nova Southeastern University.
8
Smithsonian Conservation Biology Institute, National Zoological Park, Front Royal, VA.
9
CIIMAR/CIMAR, Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Porto, Portugal Department of Biology, Faculty of Sciences, University of Porto, Porto, Portugal aantunes@ciimar.up.pt.

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.

KEYWORDS:

adaptation; birds; olfactory receptors; selection

PMID:
26219582
DOI:
10.1093/molbev/msv155
[Indexed for MEDLINE]

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