Experimental test of the influence of light availability on the evolution of eye size and behaviour in Daphnia

There exists extensive variation in eye size. Much work has provided a connection between light availability and differences in eye size across taxa. Experimental tests of the role of the light environment on the evolution of eye size are lacking. Here, we performed a selection experiment that examined the influence of light availability on shifts in eye size and the connection between eye size and phototactic (anti-predator) behaviour in Daphnia. We set-up replicate experimental populations of Daphnia, repeatedly evaluated phenotypic shifts in eye size during the ~50-day experiment, and performed a common garden experiment at the end of the experiment to test for evolutionary shifts in eye size and behaviour. Our phenotypic analyses showed that eye size rapidly diverged between the light treatments; relative eye size was consistently larger in the low versus high light treatments. Selection on eye size was also modified by variation in density as increases in Daphnia density favoured a larger eye. However, we did not observe differences in eye size between the light treatments following two generations of common garden rearing at the end of the experiment. We instead observed strong shifts in anti-predator behaviour. Daphnia from the low light treatment exhibited decreased phototactic responses to light. Our results show that decreased light relaxes selection on anti-predator behaviour. Such trends provide new insights into selection on eye size and behaviour.     

The pineal eye inXenopus laevis embryos and larvae: A photoreceptor with a direct excitatory effect on behaviour

Summary Behavioural experiments demonstrate that embryos and young larval stages ofXenopus laevis when exposed to a sudden drop in light intensity may show locomotor activity. Recordings from motoneurone axons demonstrate that the integrity of the pineal eye photoreceptors are essential for this response to occur. Thus the pineal has a direct excitatory effect on behaviour.The pineal eye arises embryologically as a single dorsal vesicular evagination of the diencephalon and anatomically it is very similar to that of other developing amphibians.Recording from the pineal eye using a suction electrode demonstrates that suddenly lowering the light intensity evokes a burst of impulses followed by a raised firing frequency. Conversely, increasing the light intensity leads to a lowered firing frequency. With prolonged exposure to white light at a range of intensities, the frequency of spike discharge is dependent upon the light intensity. The pineal eye can therefore act as a luminance detector.The pineal photoreceptors are most sensitive to light of a wavelength near 520 nm, this probably enables maximum sensitivity to the wavelengths of light that penetrate the freshwater environment.The possible role of the pineal eye in controlling locomotor activity is discussed.Abbreviations HRP horse raddish peroxidase - SEM scanning electron microscopy     

Comparative analysis of the size and shape of the lizard eye

Lizards occupy both scotopic (light-limited) and photopic (light-rich) environments, thereby making this clade ideal for analyses of eye morphology adaptations. This study examines how in lizards the morphology of the eye varies according to activity in these different light environments. Measurements were collected on corneal diameters and axial lengths of the eye for 239 specimens of 116 lizard species (including Sphenodon) that include both species with scotopic and photopic visual adaptations. I show that the light level available to a lizard for vision has a significant effect on eye shape and size. Scotopic lizards have eye shapes that are optimized for visual sensitivity, with larger corneal diameters relative to axial lengths. However, photopic lizards do not exhibit absolutely larger axial lengths than do scotopic lizards, and the groups have the same absolute axial lengths of the eye. Results also indicate that the light level the lizard functions under is a more significant influence on eye shape, as defined by the relationship between corneal diameter and axial length of the eye, than is phylogeny.     

Why do birds sleep with one eye open? Light exposure of the chick embryo as a determinant of monocular sleep.

Together with some aquatic mammals, birds exhibit a unique behavioral and electrophysiological state called "unihemispheric sleep," in which one cerebral hemisphere is awake and the other is sleeping. Slow-wave sleep in one hemisphere is associated with closure of the contralateral eye, while the eye contralateral to the awake hemisphere is open; closure of both eyes, in contrast, is associated with bihemispheric slow-wave sleep or with REM sleep. During the last few days of incubation, the chick's embryo is turned in the egg so that it occludes its left eye, whereas light entering through the shell can stimulate the right eye. Here we show that in the first two days after hatching, chicks coming from eggs incubated in the light prevalently slept with their right eye open, whereas those coming from eggs incubated in the dark prevalently slept with their left eye open. Thus, asymmetric light stimulation in the embryo can modulate the left-right direction of eye opening during post-hatching monocular sleep.     

Ecological constraints on sensory systems: compound eye size in Daphnia is reduced by resource limitation

Eye size is an indicator of visual capability, and macroevolutionary patterns reveal that taxa inhabiting dim environments have larger eyes than taxa from bright environments. This suggests that the light environment is a key driver of variation in eye size. Yet other factors not directly linked with visual tasks (i.e., non-sensory factors) may influence eye size. We sought to jointly investigate the roles of sensory (light) and non-sensory factors (food) in determining eye size and ask whether non-sensory factors could constrain visual capabilities. We tested environmental influences on eye size in four species of the freshwater crustacean Daphnia, crossing bright and dim light levels with high and low resource levels. We measured absolute eye size and eye size relative to body size in early and late adulthood. In general, Daphnia reared on low resources had smaller eyes, both absolutely and relatively. In contrast to the dominant macroevolutionary pattern, phenotypic plasticity in response to light was rarely significant. These patterns of phenotypic plasticity were true for overall diameter of the eye and the diameter of individual facets. We conclude that non-sensory environmental factors can influence sensory systems, and in particular, that resource availability may be an important constraint on visual capability.     

An apposition‐like compound eye with a layered rhabdom in the small diving beetle Agabus japonicus (Coleoptera,Dytiscidae)

The fine structure of the compound eyes of the adult diving beetle Agabus japonicus is described with light, scanning, and transmission electron microscopy. The eye of A. japonicus is mango‐shaped and consists of about 985 ommatidia. Each ommatidium is composed of a corneal facet lens, an eucone type of crystalline cone, a fused layered rhabdom with a basal rhabdomere, seven retinula cells (including six distal cells and one basal cell), two primary pigment cells and an undetermined number of secondary pigment cells that are restricted to the distalmost region of the eye. A clear‐zone, separating dioptric apparatus from photoreceptive structures, is not developed and the eye thus resembles an apposition eye. The cross‐sectional areas of the rhabdoms are relatively large indicative of enhanced light‐sensitivity. The distal and central region of the rhabdom is layered with interdigitating microvilli suggesting polarization sensitivity. According to the features mentioned above, we suggest that 1) the eye, seemingly of the apposition type, occurs in a taxon for which the clear‐zone (superposition) eye is characteristic; 2) the eye possesses adaptations to function in a dim‐light environment; 3) the eye may be sensitive to underwater polarized light or linearly water‐reflected polarized light. J. Morphol. 275:1273–1283, 2014. © 2014 Wiley Periodicals, Inc.     

The evolution of vertebrate eye size across an environmental gradient: phenotype does not predict genotype in a Trinidadian killifish

Vertebrates exhibit substantial variation in eye size. Eye size correlates positively with visual capacity and behaviors that enhance fitness, such as predator avoidance. This foreshadows a connection between predation and eye size evolution. Yet, the conditions that favor evolutionary shifts in eye size, besides the well‐known role for light availability, are unclear. We tested the influence of predation on the evolution of eye size in Trinidadian killifish, Rivulus hartii. Rivulus are located across a series of communities where they coexist with visually oriented piscivores ("high predation" sites), and no predators (“Rivulus‐only” sites). Wild‐caught Rivulus from high predation sites generally exhibited a smaller relative eye size than communities that lack predators. Yet, such differences were inconsistent across rivers. Second‐generation common garden reared fish revealed repeatable decreases in eye size in Rivulus from high predation sites. We performed additional experiments that tested the importance of light and resources on eye size evolution. Sites that differ in light or resource availability did not differ in eye size. Our results argue that differences in predator‐induced mortality underlie genetically‐based shifts in vertebrate eye size. We discuss the drivers of eye size evolution in light of the nonparallel trends between the phenotypic and common garden results.     

PHOTIC STIMULATION AND LEG MOVEMENTS IN THE CRAYFISH

When Cambarus clarkii is exposed to a source of light so that both eyes are equally illuminated, leg movements of the two sides are equal in frequency and amplitude. On covering one eye and exposing the uncovered eye to light, leg movements on the side of the uncovered eye are more frequent and are of greater amplitude than on the side of the covered eye. On covering the exposed eye also the leg movements on the two sides again tend to become equal in frequency and amplitude. When one eye is lost and the other remains functional, the leg movements on the side of the lost eye will be similar to those on the side of a normal, covered eye.     

Quantitative Studies on Pigment Migration and Light Sensitivity in the Compound Eye at Different Light Intensities

Comparative electrophysiological and histological studies were made on the functional significance of the secondary iris pigment migration for the sensitivity of the eye in the noctuid moth Cerapteryx graminis. The pigment position at different adapting light intensities was studied as well as the influence of different positions on the sensitivity of the eye. Adapting light intensities above a certain value hold the pigment in light position. At a 3 log units lower intensity the pigment is brought into dark position and at light intensities between these limiting values the pigment attains intermediate positions. The results indicate that at light intensities between the limiting values the pigment shifts closely follow the changes in intensity of the environmental light. With the pigment in dark position the eye is about 1000 times more sensitive than when the pigment is in light position, there being a close relationship between the sensitivity of the eye and the position of the pigment at intermediate positions.     

Expression of UV-sensitive parapinopsin in the iguana parietal eyes and its implication in UV-sensitivity in vertebrate pineal-related organs

The pineal-related organs of lower vertebrates have the ability to discriminate different wavelengths of light. This wavelength discrimination is achieved through antagonistic light responses to UV or blue and visible light. Previously, we demonstrated that parapinopsin underlies the UV reception in the lamprey pineal organ and identified parapinopsin genes in teleosts and frogs of which the pineal-related organs were reported to discriminate light. In this study, we report the first identification of parapinopsin in the reptile lineage and show its expression in the parietal eye of the green iguana. Spectroscopic analysis revealed that iguana parapinopsin is a UV-sensitive pigment, similar to lamprey parapinopsin. Interestingly, immunohistochemical analyses using antibodies specific to parapinopsin and parietopsin, a parietal eye green-sensitive pigment, revealed that parapinopsin and parietopsin are colocalized in the outer segments of the parietal eye photoreceptor cells in iguanas. These results strongly suggest that parapinopsin underlies the wavelength discrimination involving UV reception in the iguana parietal eye. The current findings support the idea that parapinopsin is a common photopigment underlying the UV-sensitivity in wavelength discrimination of the pineal-related organs found from lampreys to reptiles.     

Immunochemical evidence for the light-regulated modulation of phosphatidylinositol-4,5-bisphosphate in rat photoreceptor cells

Immunocytochemical localization of phosphatidylinositol-4,5-bisphosphate (PIP2) in the rat rod photoreceptor outer segments (OS) was investigated with rabbit antiPIP2 antibodies. The OS of the light-adapted rat eye showed little or no staining, whereas the OS of the dark-adapted eye were intensely stained for PIP2. The immunoreactivity of photoreceptor PIP2 in the eye exposed to a brief flash of light was markedly reduced. However, subsequent dark-adaptation of the flash-bleached eye resulted in a rapid recovery of PIP2 immunoreactivity; dark-adaptation for 5 min was sufficient for recovery to the fully dark-adapted level. In dark-adapted eyes exposed to graded light intensities, the PIP2 immunostaining varied with light levels and was correlated with unbleached rhodopsin concentrations. These results suggest that PIP2 in the rat photoreceptor cells is rapidly hydrolyzed upon light exposure and rapidly synthesized in the dark and that the decrease of PIP2 level is triggered by photic bleaching of rhodopsin.     

A specialized dorsal rim area for polarized light detection in the compound eye of the scarab beetle Pachysoma striatum

Many animals have been shown to use the pattern of polarized light in the sky as an optical compass. Specialised photoreceptors are used to analyse this pattern. We here present evidence for an eye design suitable for polarized skylight navigation in the flightless desert scarab Pachysoma striatum. Morphological and electrophysiological studies show that an extensive part of the dorsal eye is equivalent to the dorsal rim area used for polarized light navigation in other insects. A polarization-sensitivity of 12.8 (average) can be recorded from cells sensitive to the ultraviolet spectrum of light. Features commonly known to increase the visual fields of polarization-sensitive photoreceptors, or to decrease their spatial resolution, are not found in the eye of this beetle. We argue that in this insect an optically unspecialised area for polarized light detection allows it not be used exclusively for polarized light navigation.     

超连续谱激光可见谱段致人眼眩目效应研究

本文采用超连续谱激光光源滤除其红外部分仅输出可见谱段部分,在不超过国家安全标准允许的最大辐照量条件下,以正入射方式照射人眼后,记录并分析在明、暗适应条件下中心极限视力恢复时间、中心近极限视力恢复时间和视觉后像持续时间,明确超连续谱激光可见谱段对人眼的眩目效果。明适应下激光照射0.1 s导致人眼中心极限视力恢复时间为31~119 s,中心近极限视力恢复时间为19~76 s;暗适应下激光照射0.1 s导致人眼中心极限视力恢复时间为26~223 s,中心近极限视力恢复时间为13~123 s;明、暗适应下导致人眼眩目效应的最小功率密度值分别为0.055 mW/cm^2和0.005 mW/cm^2。结果表明,超连续谱激光可见谱段对人眼有良好的眩目效果,可导致数十秒至数百秒的中心视力下降,随着照射功率密度增高,眩目效应增强,显示出较好的量效关系,且相同功率密度时暗适应下人眼的眩目效果优于明适应。该研究探究了明、暗适应条件下超连续谱激光对人眼眩目效应,明确了超连续谱激光与人眼眩目的量效关系。     

Sexual Dimorphism in the Compound Eye of Rhagophthalmus ohbai (Coleoptera: Rhagophthalmidae): II. Physiology and Function of the Eye of the Male

The eyes of male and female Rhagophthalmus ohbai are of very different sizes and possess approximately 3000 and 35 facets, respectively. In the male eye one can distinguish a smaller dorsal region with 500 facets and a larger ventral one with ca. 1800. Ultrastructural differences between them have been described earlier in this journal (Lau and Meyer-Rochow, 2006). Electrophysiological recordings from the two eye areas have now revealed that the ventral region is maximally sensitive to light of 600 nm wavelength, while the dorsal eye region responds maximally to light of 540–560 nm wavelengths. In the dorsal eye region sensitivity to UV-radiation at around 360 nm wavelength, being twice as high as that of the ventral eye region, amounted to ca. one quarter of peak wavelength sensitivity. The regional differences in spectral sensitivity seem to be a reflection of the different tasks of the two eye regions: looking downward to see the yellow light emitted by a female, sensitivity towards longer wavelengths would be advantageous, but looking upward into the twilight sky, sensitivity to shorter wavelength would be a more appropriate adaptation.     

Does a biological clock reside in the eye of quail?

The site (intra- vs. extraocular) of the circadian clock driving an ocular melatonin rhythm in Japanese quail was investigated by alternately covering the left and right eyes of individual quail, otherwise held in constant light (LL), for 12-hr periods. This procedure exposed each eye to a light-dark (LD) 12:12 light cycle 180 degrees (12 hr) out of phase with the LD 12:12 light cycle experienced by the other eye. This protocol entrained the melatonin rhythm in the left eye of quail 180 degrees out of phase with the rhythm expressed in the right eye. These results are compatible with the hypothesis that an independent light-entrainable circadian pacemaker resides in each eye; they are incompatible with the hypothesis that a single (or functionally single) extraocular pacemaker drives the ocular melatonin rhythm in both eyes. However, the results are also compatible with a model in which two independent extraocular circadian pacemakers, each with an exclusive photic input from one eye, drive the ocular melatonin rhythm.     

Effects of duration and intensity of illumination on several parameters of the chick eye

Effects of duration and intensity of illumination on eye weight, eye diameter, corneal diameter and anterior chamber depth were investigated in Warren chicks. Increase in eye weight was observed in continuous light, LD 22:2 and continuous darkness. Shallow anterior chamber and small corneal diameter were observed in continuous light and LD 22:2, but not in continuous darkness. Continuous bright light (5000 lux) did not induce an increase in the eye weight but instead induced severe lesions in the anterior segment of the eye. Injection of corticosterone (500 micrograms) induced a significant reduction in the eye weight.     

Retinal and optical adaptations for nocturnal vision in the halictid bee<Emphasis Type="Italic"> Megalopta genalis</Emphasis>

The apposition compound eye of a nocturnal bee, the halictid Megalopta genalis, is described for the first time. Compared to the compound eye of the worker honeybee Apis mellifera and the diurnal halictid bee Lasioglossum leucozonium, the eye of M. genalis shows specific retinal and optical adaptations for vision in dim light. The major anatomical adaptations within the eye of the nocturnal bee are (1) nearly twofold larger ommatidial facets and (2) a 4–5 times wider rhabdom diameter than found in the diurnal bees studied. Optically, the apposition eye of M. genalis is 27 times more sensitive to light than the eyes of the diurnal bees. This increased optical sensitivity represents a clear optical adaptation to low light intensities. Although this unique nocturnal apposition eye has a greatly improved ability to catch light, a 27-fold increase in sensitivity alone cannot account for nocturnal vision at light intensities that are 8 log units dimmer than during daytime. New evidence suggests that additional neuronal spatial summation within the first optic ganglion, the lamina, is involved.B.G. is thankful for travel awards from the Royal Physiographic Society, the Per Westlings Fond, the Foundation of Dagny and Eilert Ekvall and the Royal Swedish Academy of Sciences. E.J.W. is grateful for the support of a Smithsonian Short-Term Research Fellowship, the Swedish Research Council, the Crafoord Foundation, the Wenner-Gren Foundation and the Royal Physiographic Society of Lund for their ongoing support     

Properties of visual cells in the lateral eye of Limulus in situ.

Excitatory properties of visual cells in the lateral eye of Limulus, investigated by optic nerve recordings in situ, differ significantly from the properties of cells in the classical, excised eye preparation. The differences suggest the possibility that two receptor mechanisms function in the eye in situ: one mechanism encodes low light intensities and the other responds to high intensities. The two mechanisms enable each ommatidium to respond over an intensity range of approximately 10 log units. This hypothesis was tested by measuring the increment threshold and the spectral sensitivity, by studying light and dark adaptation, and by analyzing the variability of the impulse discharge. Although the results do not conclusively identify two receptor mechanisms, they indicate that a process or a part of a process that functions in the eye in situ is abolished by excising the eye or cutting off its blood supply.     

夜蛾复眼转化速度与光暗适应的时间关系

夜行蛾类的复眼,随光、暗适应时间而逐步转化,这种转化是可逆的.以屏蔽色素分布范围的大小为指标来判断复眼的转化速度得以下结果:1.从亮眼到暗眼:亮眼进入暗适应后其屏蔽色素随暗适应时间的增加而逐步向远心端方向集中.屏蔽色素的移动是减速进行的.暗适应开始后的前3分钟,每分钟移动百分率为10.7,当暗到10—15分钟时每分钟移动百分率为4.6,再暗到60—150分钟时每分钟移动百分率为0.7.屏蔽色素移动的速度个体间差异较大,完成全过程大多数个体需150分钟,少数个体只需60分钟,另有个别个体经过270分钟暗适应仍尚未完成全过程.2.从暗眼到亮眼:暗眼受光后,其屏蔽色素随光适应时间的增加而向近心端方向扩散,色素移动速度随时间的增加而减缓.转化全过程约需60分钟.     

神经重叠复眼感杆光导的模式与性特化光感受器

采用反向照明的角膜中和方法,光镜下观察了活体家蝇和华虻神经重叠复眼感杆光导的模式.结果表明:其模式不仅与复眼的适应状态有关,而且与复眼的性特化区以及它的性别有关,这一结果用电镜方法得到证实.本文讨论了Boschek和Franceschini等不同研究结果和神经重叠复眼两个亚视觉系统的概念.