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

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.

Genomic insight into the nocturnal adaptation of the black-crowned night heron (Nycticorax nycticorax)

“…cochlearius , are associated with morphologies or functions of ( FOXP2 ) [ 49 ], lens ( SMAD3 ) [ 50 ], cornea ( SLC4A10 ) [ 51 ], retina ( EPAS1 ) [ 52 ], and optic nerve ( OPA1 ) [ 53 , 54 ], respectively. Relaxed selection of these genes may contribute to adjust the morphologies or functions of different eye components to enhance night vision as the finding in a previous study of barn owl ( Tyto alba ) [ 35 ]. In the barn owl, the unique phenotypes of the scotopic-adapted eyes are hypothesized to have evolved through relaxed or intensified selection in genes with predominant roles in different eye elements [ 35 ].…”

“…Relaxed selection of these genes may contribute to adjust the morphologies or functions of different eye components to enhance night vision as the finding in a previous study of barn owl ( Tyto alba ) [ 35 ]. In the barn owl, the unique phenotypes of the scotopic-adapted eyes are hypothesized to have evolved through relaxed or intensified selection in genes with predominant roles in different eye elements [ 35 ]. Additionally, the authors suggested that some genes have coevolved with contrasting selective signature due to adaptive compensation [ 35 ].…”

Not like night and day: the nocturnal letter-winged kite does not differ from diurnal congeners in orbit or endocast morphology

“…[ 48 ] and Borges et al . [ 49 ] and used Materialise Mimics angle, distance and plane tools. Orbital margin convergence (OMC) was calculated using the orbit posterior angle (OPA).…”

Genomic Evidence for Sensorial Adaptations to a Nocturnal Predatory Lifestyle in Owls

“…2018) . In birds, the genetic basis for nocturnal adaptations has mostly been studied in the visual system of two nocturnal species, the kiwi Apteryx mantelli and the barn owl Tyto alba ( Borges et al 2015 , 2019 ; Le Duc et al 2015 ; Emerling 2018) . Le Duc et al (2015) showed that adaptations to nocturnality in kiwis are associated with an increase in the olfactory receptor repertoire and an accumulation of evolutionary changes in genes related to color vision, mitochondrial function, and energy expenditure.…”