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BMC Genomics. 2015 Oct 6;16:751. doi: 10.1186/s12864-015-1924-3.

Gene loss, adaptive evolution and the co-evolution of plumage coloration genes with opsins in birds.

Author information

1
CIIMAR/CIMAR, Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Rua dos Bragas, 177, 4050-123, Porto, Portugal. ruiborges23@gmail.com.
2
Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre, 4169-007, Porto, Portugal. ruiborges23@gmail.com.
3
CIIMAR/CIMAR, Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Rua dos Bragas, 177, 4050-123, Porto, Portugal. btimran@gmail.com.
4
Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre, 4169-007, Porto, Portugal. btimran@gmail.com.
5
Smithsonian Conservation Biology Institute, National Zoological Park, 1500 Remount Road, Front Royal, VA, 22630, USA. johnsonwe@si.edu.
6
Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Volgade 5-7, 1350, Copenhagen, Denmark. mtpgilbert@gmail.com.
7
China National GeneBank, BGI-Shenzhen, Shenzen, 518083, China. zhanggj@genomics.cn.
8
Centre for Social Evolution, Department of Biology, Universitetsparken 15, University of Copenhagen, DK-2100, Copenhagen, Denmark. zhanggj@genomics.cn.
9
Department of Neurobiology, Duke University Medical Center Durham, Box 3209, North Carolina, 27710, USA. jarvis@neuro.duke.edu.
10
Howard Hughes Medical Institute, Chevy Chase, Maryland, 20815, USA. jarvis@neuro.duke.edu.
11
Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, St. Petersburg, 199004, Russia. lgdchief@gmail.com.
12
Oceanographic Center, Nova Southeastern University, 8000 N. Ocean Drive, Ft Lauderdale, Florida, 33004, USA. lgdchief@gmail.com.
13
CIIMAR/CIMAR, Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Rua dos Bragas, 177, 4050-123, Porto, Portugal. aantunes@ciimar.up.pt.
14
Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre, 4169-007, Porto, Portugal. aantunes@ciimar.up.pt.

Abstract

BACKGROUND:

The wide range of complex photic systems observed in birds exemplifies one of their key evolutionary adaptions, a well-developed visual system. However, genomic approaches have yet to be used to disentangle the evolutionary mechanisms that govern evolution of avian visual systems.

RESULTS:

We performed comparative genomic analyses across 48 avian genomes that span extant bird phylogenetic diversity to assess evolutionary changes in the 17 representatives of the opsin gene family and five plumage coloration genes. Our analyses suggest modern birds have maintained a repertoire of up to 15 opsins. Synteny analyses indicate that PARA and PARIE pineal opsins were lost, probably in conjunction with the degeneration of the parietal organ. Eleven of the 15 avian opsins evolved in a non-neutral pattern, confirming the adaptive importance of vision in birds. Visual conopsins sw1, sw2 and lw evolved under negative selection, while the dim-light RH1 photopigment diversified. The evolutionary patterns of sw1 and of violet/ultraviolet sensitivity in birds suggest that avian ancestors had violet-sensitive vision. Additionally, we demonstrate an adaptive association between the RH2 opsin and the MC1R plumage color gene, suggesting that plumage coloration has been photic mediated. At the intra-avian level we observed some unique adaptive patterns. For example, barn owl showed early signs of pseudogenization in RH2, perhaps in response to nocturnal behavior, and penguins had amino acid deletions in RH2 sites responsible for the red shift and retinal binding. These patterns in the barn owl and penguins were convergent with adaptive strategies in nocturnal and aquatic mammals, respectively.

CONCLUSIONS:

We conclude that birds have evolved diverse opsin adaptations through gene loss, adaptive selection and coevolution with plumage coloration, and that differentiated selective patterns at the species level suggest novel photic pressures to influence evolutionary patterns of more-recent lineages.

PMID:
26438339
PMCID:
PMC4595237
DOI:
10.1186/s12864-015-1924-3
[Indexed for MEDLINE]
Free PMC Article

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