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Avian Binocularity and Adaptation to Nocturnal Environments: Genomic Insights from a Highly Derived Visual Phenotype.

Publication ,  Journal Article
Borges, R; Fonseca, J; Gomes, C; Johnson, WE; O'Brien, SJ; Zhang, G; Gilbert, MTP; Jarvis, ED; Antunes, A
Published in: Genome Biol Evol
August 1, 2019

Typical avian eyes are phenotypically engineered for photopic vision (daylight). In contrast, the highly derived eyes of the barn owl (Tyto alba) are adapted for scotopic vision (dim light). The dramatic modifications distinguishing barn owl eyes from other birds include: 1) shifts in frontal orientation to improve binocularity, 2) rod-dominated retina, and 3) enlarged corneas and lenses. Some of these features parallel mammalian eye patterns, which are hypothesized to have initially evolved in nocturnal environments. Here, we used an integrative approach combining phylogenomics and functional phenotypes of 211 eye-development genes across 48 avian genomes representing most avian orders, including the stem lineage of the scotopic-adapted barn owl. Overall, we identified 25 eye-development genes that coevolved under intensified or relaxed selection in the retina, lens, cornea, and optic nerves of the barn owl. The agtpbp1 gene, which is associated with the survival of photoreceptor populations, was pseudogenized in the barn owl genome. Our results further revealed that barn owl retinal genes responsible for the maintenance, proliferation, and differentiation of photoreceptors experienced an evolutionary relaxation. Signatures of relaxed selection were also observed in the lens and cornea morphology-associated genes, suggesting that adaptive evolution in these structures was essentially structural. Four eye-development genes (ephb1, phactr4, prph2, and rs1) evolved in positive association with the orbit convergence in birds and under relaxed selection in the barn owl lineage, likely contributing to an increased reliance on binocular vision in the barn owl. Moreover, we found evidence of coevolutionary interactions among genes that are expressed in the retina, lens, and optic nerve, suggesting synergetic adaptive events. Our study disentangles the genomic changes governing the binocularity and low-light perception adaptations of barn owls to nocturnal environments while revealing the molecular mechanisms contributing to the shift from the typical avian photopic vision to the more-novel scotopic-adapted eye.

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Published In

Genome Biol Evol

DOI

EISSN

1759-6653

Publication Date

August 1, 2019

Volume

11

Issue

8

Start / End Page

2244 / 2255

Location

England

Related Subject Headings

  • Transcriptome
  • Strigiformes
  • Phylogeny
  • Phenotype
  • Night Vision
  • Genome
  • Gene Expression Regulation, Developmental
  • Eye Proteins
  • Environment
  • Developmental Biology
 

Citation

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ICMJE
MLA
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Borges, R., Fonseca, J., Gomes, C., Johnson, W. E., O’Brien, S. J., Zhang, G., … Antunes, A. (2019). Avian Binocularity and Adaptation to Nocturnal Environments: Genomic Insights from a Highly Derived Visual Phenotype. Genome Biol Evol, 11(8), 2244–2255. https://doi.org/10.1093/gbe/evz111
Borges, Rui, João Fonseca, Cidália Gomes, Warren E. Johnson, Stephen J. O’Brien, Guojie Zhang, M Thomas P. Gilbert, Erich D. Jarvis, and Agostinho Antunes. “Avian Binocularity and Adaptation to Nocturnal Environments: Genomic Insights from a Highly Derived Visual Phenotype.Genome Biol Evol 11, no. 8 (August 1, 2019): 2244–55. https://doi.org/10.1093/gbe/evz111.
Borges R, Fonseca J, Gomes C, Johnson WE, O’Brien SJ, Zhang G, et al. Avian Binocularity and Adaptation to Nocturnal Environments: Genomic Insights from a Highly Derived Visual Phenotype. Genome Biol Evol. 2019 Aug 1;11(8):2244–55.
Borges, Rui, et al. “Avian Binocularity and Adaptation to Nocturnal Environments: Genomic Insights from a Highly Derived Visual Phenotype.Genome Biol Evol, vol. 11, no. 8, Aug. 2019, pp. 2244–55. Pubmed, doi:10.1093/gbe/evz111.
Borges R, Fonseca J, Gomes C, Johnson WE, O’Brien SJ, Zhang G, Gilbert MTP, Jarvis ED, Antunes A. Avian Binocularity and Adaptation to Nocturnal Environments: Genomic Insights from a Highly Derived Visual Phenotype. Genome Biol Evol. 2019 Aug 1;11(8):2244–2255.
Journal cover image

Published In

Genome Biol Evol

DOI

EISSN

1759-6653

Publication Date

August 1, 2019

Volume

11

Issue

8

Start / End Page

2244 / 2255

Location

England

Related Subject Headings

  • Transcriptome
  • Strigiformes
  • Phylogeny
  • Phenotype
  • Night Vision
  • Genome
  • Gene Expression Regulation, Developmental
  • Eye Proteins
  • Environment
  • Developmental Biology