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

Rui Borges, João Fonseca, Cidália Gomes, Warren E. Johnson, Stephen J. O'Brien, Guojie Zhang, M. Thomas P. Gilbert, Erich D. Jarvis, Agostinho Antunes

Research output

Abstract

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.

Original languageEnglish
Pages (from-to)2244-2255
JournalGenome Biology and Evolution
Volume11
Issue number8
DOIs
Publication statusPublished - 22 Aug 2019

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Strigiformes
Tyto alba
phenotype
genomics
Phenotype
eyes
gene
Lens
Lenses
cornea
Genes
retina
Cornea
Color Vision
genes
Optic Nerve
optics
photoreceptors
genome
Birds

Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

Cite this

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 Biology and Evolution, 11(8), 2244-2255. https://doi.org/10.1093/gbe/evz111
Borges, Rui ; Fonseca, João ; Gomes, Cidália ; Johnson, Warren E. ; O'Brien, Stephen J. ; Zhang, Guojie ; Gilbert, M. Thomas P. ; Jarvis, Erich D. ; Antunes, Agostinho. / Avian Binocularity and Adaptation to Nocturnal Environments : Genomic Insights from a Highly Derived Visual Phenotype. In: Genome Biology and Evolution. 2019 ; Vol. 11, No. 8. pp. 2244-2255.
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Borges, R, Fonseca, J, Gomes, C, Johnson, WE, O'Brien, SJ, Zhang, G, Gilbert, MTP, Jarvis, ED & Antunes, A 2019, 'Avian Binocularity and Adaptation to Nocturnal Environments: Genomic Insights from a Highly Derived Visual Phenotype', Genome Biology and Evolution, vol. 11, no. 8, pp. 2244-2255. https://doi.org/10.1093/gbe/evz111

Avian Binocularity and Adaptation to Nocturnal Environments : Genomic Insights from a Highly Derived Visual Phenotype. / Borges, Rui; Fonseca, João; Gomes, Cidália; Johnson, Warren E.; O'Brien, Stephen J.; Zhang, Guojie; Gilbert, M. Thomas P.; Jarvis, Erich D.; Antunes, Agostinho.

In: Genome Biology and Evolution, Vol. 11, No. 8, 22.08.2019, p. 2244-2255.

Research output

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