TY - JOUR

T1 - Avian Binocularity and Adaptation to Nocturnal Environments

T2 - Genomic Insights from a Highly Derived Visual Phenotype

AU - Borges, Rui

AU - Fonseca, João

AU - Gomes, Cidália

AU - Johnson, Warren E.

AU - O'Brien, Stephen J.

AU - Zhang, Guojie

AU - Gilbert, M. Thomas P.

AU - Jarvis, Erich D.

AU - Antunes, Agostinho

PY - 2019/8/22

Y1 - 2019/8/22

N2 - 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.

AB - 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.

KW - barn owl

KW - coevolution

KW - eye-development

KW - ocular adaptations

KW - pseudogenization

KW - relaxed and intensified evolution

KW - BCL11B

KW - PATTERNS

KW - MODEL

KW - DEGENERATION

KW - ACCURACY

KW - EYE

KW - EVOLUTION

KW - RETINA

KW - EXPRESSION

KW - BIRDS

UR - http://www.scopus.com/inward/record.url?scp=85071997339&partnerID=8YFLogxK

UR - http://www.mendeley.com/research/avian-binocularity-adaptation-nocturnal-environments-genomic-insights-highly-derived-visual-phenotyp

U2 - 10.1093/gbe/evz111

DO - 10.1093/gbe/evz111

M3 - Article

C2 - 31386143

AN - SCOPUS:85071997339

VL - 11

SP - 2244

EP - 2255

JO - Genome Biology and Evolution

JF - Genome Biology and Evolution

SN - 1759-6653

IS - 8

ER -