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.
Project description:Despite the large amount of variation found in the night (scotopic) vision capabilities of healthy volunteers, little effort has been made to characterize this variation and factors, genetic and non-genetic, that influence it. In the largest population of healthy observers measured for scotopic visual acuity (VA) and contrast sensitivity (CS) to date, we quantified the effect of a range of variables on visual performance. We found that young volunteers with excellent photopic vision exhibit great variation in their scotopic VA and CS, and this variation is reliable from one testing session to the next. We additionally identified that factors such as Circadian preference, iris color, astigmatism, depression, sex and education have no significant impact on scotopic visual function. We confirmed previous work showing that the amount of time spent on the vision test influences performance and that laser eye surgery results in worse scotopic vision. We also showed a significant effect of intelligence and photopic visual performance on scotopic VA and CS, but all of these variables collectively explain <30% of the variation in scotopic vision. The wide variation seen in young healthy volunteers with excellent photopic vision, the high test-retest agreement, and the vast majority of the variation in scotopic vision remaining unexplained by obvious non-genetic factors suggests a strong genetic component. Our preliminary genome-wide association study (GWAS) of 106 participants ruled out any common genetic variants of very large effect and paves the way for future, larger genetic studies of scotopic vision.
Project description:It is commonly accepted that the evolution of the human eye has been driven by the maximum intensity of the radiation emitted by the Sun. However, the interpretation of the surrounding environment is constrained not only by the amount of energy received but also by the information content of the radiation. Information is related to entropy rather than energy. The human brain follows Bayesian statistical inference for the interpretation of visual space. The maximization of information occurs in the process of maximizing the entropy. Here, we show that the photopic and scotopic vision absorption peaks in humans are determined not only by the intensity but also by the entropy of radiation. We suggest that through the course of evolution, the human eye has not adapted only to the maximum intensity or to the maximum information but to the optimal wavelength for obtaining information. On Earth, the optimal wavelengths for photopic and scotopic vision are 555?nm and 508?nm, respectively, as inferred experimentally. These optimal wavelengths are determined by the temperature of the star (in this case, the Sun) and by the atmospheric composition.
Project description:New genomic tools open doors to study ecology, evolution, and population genomics of wild animals. For the Barn owl species complex, a cosmopolitan nocturnal raptor, a very fragmented draft genome was assembled for the American species (Tyto furcata pratincola) (Jarvis et al. 2014). To improve the genome, we assembled de novo Illumina and Pacific Biosciences (PacBio) long reads sequences of its European counterpart (Tyto alba alba). This genome assembly of 1.219 Gbp comprises 21,509 scaffolds and results in a N50 of 4,615,526 bp. BUSCO (Universal Single-Copy Orthologs) analysis revealed an assembly completeness of 94.8% with only 1.8% of the genes missing out of 4,915 avian orthologs searched, a proportion similar to that found in the genomes of the zebra finch (Taeniopygia guttata) or the collared flycatcher (Ficedula albicollis). By mapping the reads of the female American barn owl to the male European barn owl reads, we detected several structural variants and identified 70 Mbp of the Z chromosome. The barn owl scaffolds were further mapped to the chromosomes of the zebra finch. In addition, the completeness of the European barn owl genome is demonstrated with 94 of 128 proteins missing in the chicken genome retrieved in the European barn owl transcripts. This improved genome will help future barn owl population genomic investigations.
Project description:BACKGROUND: Bird species show a high degree of variation in the composition of their preen gland waxes. For instance, galliform birds like chicken contain fatty acid esters of 2,3-alkanediols, while Anseriformes like goose or Strigiformes like barn owl contain wax monoesters in their preen gland secretions. The final biosynthetic step is catalyzed by wax synthases (WS) which have been identified in pro- and eukaryotic organisms. RESULTS: Sequence similarities enabled us to identify six cDNAs encoding putative wax synthesizing proteins in chicken and two from barn owl and goose. Expression studies in yeast under in vivo and in vitro conditions showed that three proteins from chicken performed WS activity while a sequence from chicken, goose and barn owl encoded a bifunctional enzyme catalyzing both wax ester and triacylglycerol synthesis. Mono- and bifunctional WS were found to differ in their substrate specificities especially with regard to branched-chain alcohols and acyl-CoA thioesters. According to the expression patterns of their transcripts and the properties of the enzymes, avian WS proteins might not be confined to preen glands. CONCLUSIONS: We provide direct evidence that avian preen glands possess both monofunctional and bifunctional WS proteins which have different expression patterns and WS activities with different substrate specificities.
Project description:Visual cues are often a vital part of animal communication and courtship. While a plethora of studies have focused on the role that hormones play in acoustic communication of anurans, relatively few have explored hormonal modulation of vision in these animals. Much of what we do know comes from behavioral studies, which show that a frog's hormonal state can significantly affect both its visual behavior and mating decisions. However, to fully understand how frogs use visual cues to make these mating decisions, we must first understand how their visual system processes these cues, and how hormones affect these processes. To do this, we performed electroretinograms (ERGs) to measure retinal sensitivity of túngara frogs (Physalaemus pustulosus), a neotropical species whose mating behavior includes previously described visual cues. To determine the effect of hormonal state on visual sensitivity, ERGs were recorded under scotopic and photopic conditions in frogs that were either non-reproductive or hormone-treated with human chorionic gonadotropin (hCG) prior to testing. Additionally, measurements of optical anatomy determined how túngara frog eye and retina morphology related to physiological sensitivity. As expected, we found that both sexes display higher visual sensitivity under scotopic conditions compared to photopic conditions. However, hormone injections significantly increased retinal sensitivity of females under scotopic conditions. These results support the hypothesis that hormonal modulation of neural mechanisms, such as those mediating visually guided reproductive behavior in this species, include modulation of the receptor organ: the retina. Thus, our data serve as a starting point for elucidating the mechanism of hormonal modulation of visual sensitivity.
Project description:Two types of photoreceptors in the human retina support vision across a wide range of luminances: cones are active under bright daylight illumination (photopic viewing) and rods under dim illumination at night (scotopic viewing). These photoreceptors are distributed inhomogeneously across the retina : cone-receptor density peaks at the center of the visual field (i.e., the fovea) and declines toward the periphery, allowing for high-acuity vision at the fovea in daylight. Rod receptors are absent from the fovea, leading to a functional foveal scotoma in night vision. In order to make optimal perceptual decisions, the visual system requires knowledge about its own properties and the relative reliability of signals arriving from different parts of the visual field . Since cone and rod signals converge on the same pathways , and their cortical processing is similar except for the foveal scotoma , it is unclear if humans can take into account the differences between scotopic and photopic vision when making perceptual decisions. Here, we show that the scotopic foveal scotoma is filled in with information from the immediate surround and that humans trust this inferred information more than veridical information from the periphery of the visual field. We observed a similar preference under daylight illumination, indicating that humans have a default preference for information from the fovea even if this information is not veridical, like in night vision. This suggests that filling-in precedes the estimation of confidence, thereby shielding awareness from the foveal scotoma with respect to its contents and its properties.
Project description:To present stimuli with varied sizes, colors, and patterns over a large range of luminance.The filter bar used in scotopic MP1 was replaced with a custom slide-in tray that introduces light from an external projector driven by an additional computer. MP1 software was modified to provide retinal tracking information to the computer driving the projector. Retinal tracking performance was evaluated by imaging the system input and the output simultaneously with a high-speed video system. Spatial resolution was measured with achromatic and chromatic grating/background combinations over scotopic and photopic ranges.The range of retinal illuminance achievable by the modification was up to 6.8 log photopic Trolands (phot-Td); however, in the current work, only a lower range over -4 to +3 log phot-Td was tested in human subjects. Optical magnification was optimized for low-vision testing with gratings from 4.5 to 0.2 cyc/deg. In normal subjects, spatial resolution driven by rods, short wavelength-sensitive (S-) cones, and long/middle wavelength-sensitive (L/M-) cones was obtained by the choice of adapting conditions and wavelengths of grating and background. Data from a patient with blue cone monochromacy was used to confirm mediation.The modified MP1 can be developed into an outcome measure for treatments in patients with severe retinal degeneration, very low vision, and abnormal eye movements such as those for whom treatment with optogenetics is planned, as well as for patients with cone disorders such as blue cone monochromacy for whom treatment with gene therapy is planned to improve L/M-cone function above a normal complement of rod and S-cone function.
Project description:In photopic vision, the border between two fields is minimally distinct when the two fields are isoluminant; that is, when the achromatic luminance of the two fields is equal. The distinctness of a border between extrafoveal reference and comparison fields was used here as an isoluminance criterion under a variety of adaptation conditions ranging from photopic to scotopic. The adjustment was done by trading off the amount of blue against the amount of red in the comparison field. Results show that isoluminant border settings are linear under all constant adaptation conditions, though varying with state of adaptation. The relative contribution of rods and cones to luminance was modeled such that the linear sum of the suitably weighted scotopic and photopic luminance is constant for the mesopic isoluminant conditions. The relative weights change with adapting intensity in a sigmoid fashion and also depend strongly on the position of the border in the visual field.
Project description:Most vertebrate retinas contain a single type of rod for scotopic vision and multiple types of cones for photopic and color vision. The retinas of certain amphibian species uniquely contain two types of rods: red rods, which express rhodopsin, and green rods, which express a blue-sensitive cone pigment (M1/SWS2 group). Spontaneous activation of rhodopsin induced by thermal isomerization of the retinal chromophore has been suggested to contribute to the rod's background noise, which limits the visual threshold for scotopic vision. Therefore, rhodopsin must exhibit low thermal isomerization rate compared with cone visual pigments to adapt to scotopic condition. In this study, we determined whether amphibian blue-sensitive cone pigments in green rods exhibit low thermal isomerization rates to act as rhodopsin-like pigments for scotopic vision. Anura blue-sensitive cone pigments exhibit low thermal isomerization rates similar to rhodopsin, whereas Urodela pigments exhibit high rates like other vertebrate cone pigments present in cones. Furthermore, by mutational analysis, we identified a key amino acid residue, Thr47, that is responsible for the low thermal isomerization rates of Anura blue-sensitive cone pigments. These results strongly suggest that, through this mutation, anurans acquired special blue-sensitive cone pigments in their green rods, which could form the molecular basis for scotopic color vision with normal red rods containing green-sensitive rhodopsin.
Project description:Danon disease is a neuromuscular disorder with variable expression in the eye. We describe a family with Danon disease and cone-rod dystrophy (CRD).Affected males of one family with Danon were invited for an extensive ophthalmologic examination, including color vision testing, fundus photography, Goldmann perimetry, full-field electroretinogram (ERG), and SD-OCT. Previous ophthalmologic data were retrieved from medical charts. The LAMP2 and RPGR gene were analyzed by direct sequencing.Two siblings had no ocular phenotype. The third sibling and a cousin developed CRD leading to legal blindness. Visual acuity deteriorated progressively over time, color vision was severely disturbed, and ERG showed reduced photopic and scotopic responses. SD-OCT revealed thinning of the photoreceptor and RPE layer. Visual fields demonstrated central scotoma. The causal mutation was p.Gly384Arg in LAMP2; no mutations were found in RPGR.This is the first description of CRD in Danon disease. The retinal phenotype was a late onset but severe dystrophy characterized by loss of photoreceptors and RPE cells. With this report, we highlight the importance of a comprehensive ophthalmologic examination in the clinical work-up of Danon disease.