Energy Flow 3. Carbon Cycling 4. Climate Change 5: Evolution 1. Evolution Evidence 2. Natural Selection 3. Classification 4. Cladistics 6: Human Physiology 1. Digestion 2. The Blood System 3. Disease Defences 4. Gas Exchange 5. Homeostasis Higher Level 7: Nucleic Acids 1.
DNA Structure 2. Transcription 3. Biological clocks that maintain regular physiological cycles — and cause the discomforts of jet lag — nearly always are controlled by these photoreceptors. Skin photoreceptors like those in fish or octopus often control color and pattern variations. This capacity is based on the cryptochromes, which apparently underlie mechanisms for magnetic orientation in animals as different as birds and cockroaches.
With the discovery of light-sensitive retinal cells in addition to rods and cones in mammalian retinas, it became obvious that humans, too, must use nonvisual pathways for control of behavior and function. Pupil size varies with changing light, even in functionally blind humans.
A joint British-American study, published in , found that patients who have lost all rods and cones due to genetic disorders can still have light-responsive daily rhythms and pupils. Finally, an unexpected recent finding in research led by Solomon Snyder and Dan Berkowitz , also at Johns Hopkins University, found that blood vessels in mice contain melanopsin, the opsin used in retinal nonvisual photoreception.
Since humans are likely to have the same system, this could partially explain the increase in heart attacks in the morning , which are perhaps associated with blood pressure changes occurring at that time. We know nonvisual light detection is ubiquitous and significant in the lives of animals. Future research will continue to untangle its effects on human health and well-being. This article was originally published on The Conversation. Read the original article.
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The results were unexpected figure 4 ; see electronic supplementary material. Non-directional photoreception for detecting the diel light cycle can accommodate the full, 8 log unit range of luminance without any morphological membrane specializations.
Even if the photopigment density is several log units lower than in vertebrate or insect visual cells, the sensitivity would be high enough to detect moonlight.
For non-visual luminance monitoring, there is thus no need for cilia or microvilli. Indeed, non-visual photoreceptors often lack these conspicuous structures altogether Gooley et al.
Modelling also demonstrates that phototaxis, which requires directionality with wide angular sensitivities and intermediate integration times, can function without membrane stacking, but only during the day, and in rather shallow water figure 4 ; see table S1, electronic supplementary material.
The fact that acoel flatworms have ocelli without cilia or rhabdomeres supports the conclusion that directional photoreception presumably for phototaxis does not require membrane stacking Yamasu For use at low crepuscular intensities in deeper water or in very turbid water, moderate stacking of membrane will help extend the range of intensities where phototaxis can be used figure 4. Directionality, fast response and adaptation acting as a temporal high-pass filter are important properties for a photoreceptor that serves phototaxis or functions as an optical statocyst figure 5.
These properties pass information about the angular distribution of light in the environment and remove information about the general ambient luminance.
A photoreceptor cell that develops a role for directional light measurements must, therefore, abandon any original task for monitoring the general ambient luminance. But because entrainment of biological clocks is likely to remain important, directional photoreception would probably only evolve after a non-directional photoreceptor has been duplicated.
The evolution of phototaxis and optical statocysts are thus likely to have served as early reasons for multiple photoreceptor systems in early metazoans. Key innovations in eye evolution. Directional photoreception is assumed to have evolved from non-directional monitoring of ambient luminance by a cell duplication event and an opsin gene duplication leading to a receptor opsin and photoisomerase pair of proteins for efficient chromophore regeneration.
This was followed by the introduction of screening pigment and soon also by membrane stacking to allow for better contrast discrimination, increased speed and more directional photoreception. Multiple receptor cells would then allow for true spatial vision and the scanning mode of operation could be abandoned. The single-chambered and compound eyes would have to evolve independently from directional ocelli. To collect enough photons for spatial vision with higher resolution, lenses must be introduced, but the new high-resolution tasks are expected to add to rather than replace the older low-resolution tasks.
A single directional photoreceptor relies on body movement to acquire information about the angular spatial distribution of light, and this interferes with the ability to detect changes in the environment.
With different photoreceptors pointing in different directions, spatial information can be collected simultaneously without body movement. With just two receptors pointing in different directions, there is in principle an image, and by adding more receptors, the eye can increase the amount of information virtually without limit.
Spatial vision is also the most information rich of all senses, and it offers sensory guidance to the most sophisticated of animal behaviours. There can be no doubt that the step from a directional photoreceptor to the first pit or cup eye was of pivotal importance for animal evolution. Evolving a spatially resolving eye from a directional photoreceptor means that the angle seen by each receptor will have to shrink, and this dramatically reduces the rate at which photons are detected.
This loss in sensitivity is a major obstacle in the evolution of spatial vision. The problem is compounded by the fact that the integration time will have to be reduced along with the receptor's field of view in order to keep motion blur at tolerable levels. In addition, the contrasts of interest are smaller for spatial vision than for phototaxis, which calls for larger photon samples per integration time see electronic supplementary material for a discussion of photon sample size.
A consequence of this rapidly increasing need for photons is that stacking of the photoreceptor membrane becomes an absolute prerequisite for the evolution of spatial vision. Even daylight would be too dim for a pigment-cup eye without any stacking of the photoreceptive membrane figure 4 ; table S1, electronic supplementary material.
Rhabdoms and ciliary specializations must thus have been in place, at least to some degree, before the first spatially resolving eyes evolved. Because each double membrane layer can absorb not more than 0. But when the membrane layers become numerous, the gain produced by each new layer declines.
A human rod has some discs, and a blowfly rhabdom has about twice that number of microvillar layers. Compared with an unfolded cell membrane, this stacking involves a sensitivity gain of 2—3 log units see equations in electronic supplementary material.
If such a sensitivity gain were spent on compensating for the sensitivity loss caused by decreasing angular sensitivities, how much spatial resolution would it buy? The answer is somewhat disappointing.
After exhausting the benefits brought about by membrane stacking, another strategy is obviously necessary for continued refinement of visual resolution.
That strategy is the introduction of focusing optics. By introducing a lens, the area detecting light can be shifted from the area of the receptor cell to the area of a lens figure 4 ; table S1, electronic supplementary material. This allows for a huge boost in photon catch, which is needed for the high resolution of arthropod, cephalopod and vertebrate eyes, and it provides enough sensitivity to tune eye design to nocturnal or deep-sea use.
Lenses can be introduced gradually if there is tissue filling the cavity of a pigment-cup eye figure 1 e. Recent work on the eyes of box jellyfish O'Connor et al. Before focusing properties evolve, the obvious way to form an image is by shading in a pigment pit or cup. A simple way of forming the pigment cup is to make the receptor cells line the exterior of a growing lump of transparent cells. Such a mechanical function would require some rigidity of the transparent cells, and this would naturally pre-adapt the cup eye for transition to a lens eye.
Another and possibly even older function of vitreous cells in the cavity of pit or cup eyes is to serve as UV filters for protecting against radiation damage to the receptor cells. Spatial vision can originate not only by multiplying receptor cells inside a pigment pit, but an equally viable option is to multiply the entire structure including the pigment pit.
In flatworms, these two possibilities are both represented Kuchiiwa et al. At early stages of eye evolution, it is not easy to see that either of the two alternatives would be much better than the other.
Later, however, when lenses have been introduced, the single chambered solution turns out to outperform the compound eye by a rather wide margin Kirschfeld One reason for the difference is that, in eyes of comparable size, the many lenses of a compound eye must be much smaller than the single lens in a camera type eye.
The approximately 1. This means that information about the absolute intensity is removed from the visual system. Yet, some mechanisms of adaptation, such as the pupil diameter and the amount of neural summation Warrant , should ideally be controlled by the absolute intensity. As a consequence, non-visual photoreception serves a function in imaging eyes, and it is no surprise that visual interneurons, such as some ganglion cells in vertebrate eyes, are intrinsically light sensitive, without directly contributing to vision Gooley et al.
These cells display similarities to other non-visual photoreceptors in the slow time course of the response Do et al. For an evolutionary understanding of intrinsically light-sensitive interneurons in the visual pathway, it is important to note that this non-visual function is likely to represent an elaboration of the visual pathway, and, as such, it is not necessarily a conserved function dating back to pre-visual ancestors.
The driving force behind sensory evolution is the addition of new sensory tasks that provide animals with new responses to external information. This reasoning leads to an understanding of sensory evolution as a task-punctuated process.
For the evolution of each new task, the sensory system will be subject to selection that works towards extraction of a specific subset of sensory information.
New sensory tasks evolve by modification or elaboration of systems that serve already existing sensory tasks. In some cases, the new task serves a similar purpose as an older task, leading to the replacement and loss of the older task. An example of replacement is the transition from directional photoreceptors used for phototaxis to spatial vision with multiple photoreceptors.
Here, it is likely that the ancestral scanning mode of data acquisition was simply replaced by the simultaneous acquisition of spatial information. In other cases, a new task was introduced without making the previous task obsolete. The evolution of directional photoreception for phototaxis from non-directional monitoring of the diel light cycle is an obvious example in which the new sensory task does not infringe on the value of the older task.
In such cases, a duplication event must have initiated the evolution of the new task. On the assumption that evolution, in general, would proceed from tasks with small demands on molecular machinery and morphological structures to tasks with gradually more extensive requirements, the evolutionary sequence of early tasks leading to true vision can be reconstructed with some confidence. This sequence starts with non-visual photoreception for circadian control or water-depth control, followed by directional photoreception for phototaxis or body orientation, which then becomes replaced by true spatial vision.
In terms of structures, this would have corresponded to a sequence from photoreceptor cells without membrane specializations, via directional shading by screening pigment structures, either in the photoreceptor itself or in an associated cell, through to the development of membrane folding, which would open up for enough sensitivity to evolve the first true eyes with spatial vision figure 5.
The duplication events that led to the different opsin classes are likely to correspond to the introduction of new or modified sensory tasks. As argued in this paper, the original split between c-opsins and all other opsins may have generated a photoisomerase enzyme to improve the efficiency of the original opsin. If this was the case, the gene duplication may have led to improved function of an existing sensory task rather than the duplication into a new task and an old task.
Because this opsin duplication predates the split between Cnidaria and Bilateria Plachetzki et al. It is hard to see that rapid regeneration would be a crucial property of non-visual luminance monitoring, especially since adequately efficient cryptochrome-based systems probably were already in place Rubin et al. A distinct possibility is that the rapid regeneration of photopigment would have facilitated the evolution of directional photoreception. The evolution of membrane stacking, be it in the form of cilia, microvilli or diverticula, is expected to have been a prerequisite for the transition from directional photoreception to the first real eyes.
As a consequence, if stacking based on microvilli and cilia could be demonstrated to be of independent origin, it would imply that spatial vision originated more than once. Unfortunately, there has not been much development on this question since the intense debate of three decades ago Salvini-Plawen ; Vanfleteren There is an obvious risk that the type of membrane stacking has been more evolutionarily plastic than assumed and that the distinction between rhabdomeric and ciliary receptors has been given too much significance.
Hopefully, a broad comparative identification of the opsin type in photoreceptor cells will resolve this issue. This is an attractive idea, but it does not bring any clarity into why polychaetes have ciliary photoreceptors in the brain involved in circadian control Arendt et al.
This points to a much more ancient role for directional photoreception or indicates that it evolved independently in two different systems and that the directionality screening pigment was secondarily lost when one of the systems regained its original role in luminance monitoring.
Yet another possibility is that the association between photoreception and cilia did not originally arise as a means of membrane stacking, but that it is founded in an ancient functional connection between sensory control of ciliary beating.
The many cases of rhabdomeric and ciliary membrane stacking in cells that are not associated with screening pigment structures e. Purschke et al. The picture is further complicated by the simple ocelli in acoel flatworms figure 1 c , which lack membrane stacking, but are associated with a pigment cell Yamasu Acoel flatworms are believed to be basal bilaterians, and they have a direct development without planktonic larvae Ruiz-Trillo et al.
From the current knowledge, it seems that it is possible to generate an army of different hypothetical evolutionary scenarios, none of which fully or easily accounts for the different sets of photoreceptors in different groups of animals. Factors that affect the spectral absorbance of a visual pigment or the spectral sensitivity of a photoreceptor cell. Molecular factors of spectral tuning generally involve changes in the amino acids near the chromophore of a visual pigment.
Other factors include various kinds of optical filtering, including long-pass and short-pass filtering. Before going further, we need to define what part of the electromagnetic spectrum falls in the UV. Most of this range is not naturally present at the earth's surface, as a result of atmospheric absorption.
The UVB range is significant for its biological effects resulting from its absorption by proteins and nucleic acids, but animal UV-light visual sensitivity is almost entirely restricted to the UVA. Although it is true, as noted above, that most visual pigments including those of human retinas have significant photosensitivity in the UV, we and many other mammals have UV-absorbing pigments in the lens that entirely block the passage of this spectral range to the retina Douglas and Cronin, Aphakic individuals, who have had their lenses removed, are very sensitive to UV light, nearly as far as the UVB, which compromises their color vision.
This is why artificial intraocular lenses used today strongly absorb UV, much like a natural lens does. Ultraviolet light in nature. The other distinction that will be important throughout this Review is between UV photosensitivity and UV vision.
UV photosensitivity simply refers to the ability to detect UV light; as used in this paper, it means that the retina contains photoreceptor cells that absorb UV light and can transduce it to a cellular signal. UV photosensitivity is required for UV vision, but the latter term means that an animal can visualize UV patterns and recognize UV-containing images of objects, light fields and signals.
The distinction is important, because many animals respond strongly to UV stimuli, but the response is stereotyped and is different from the same animal's response to longer wavelengths most animals with such responses avoid UV or move away from a UV source, evidently interpreting such a stimulus as noxious or dangerous.
When UV is included in the color-vision system of an animal, it is discriminable from other colors and does not automatically elicit a specific response. Also, as the term implies, color vision is always associated with visual imaging and object recognition.
Many animals with UV photosensitivity, particularly invertebrates, have both wavelength-specific behaviors and color vision Menzel, ; see also Kelber and Osorio, Animals detect light through a phototransduction cascade mediated by visual pigments sequestered in the membranes of photoreceptor cells. Visual pigments are formed by the Schiff base covalent linkage of an opsin G-protein-coupled receptor with a vitamin A-derived chromophore.
Upon photon absorption, the chromophore isomerizes, causing a conformational change in the opsin protein that initiates a biochemical cascade culminating in a downstream cellular signal. UV opsin sequences are now known for many animal species, with those involved in chordate and arthropod visual systems being the best surveyed.
Of the four major clades of metazoan opsins established by Porter et al. The SWS1 clade contains all known vertebrate UV opsins implicated in visual tasks, whereas the parapinopsins, first identified in lamprey, exist in pineal-associated photoreceptive organs of non-mammalian vertebrates Koyanagi et al. These organs are thought to have diverse roles, including melatonin regulation, luminance detection and even chromatic discrimination between UV and longer wavelengths Koyanagi et al.
Among invertebrates, investigations of UV opsins involved in vision have thus far been restricted to the arthropods. The function of neuropsin is poorly understood, but it appears to play a role in circadian entrainment in some cases.
There may well be additional types of UV opsins in existence, especially among non-arthropod invertebrate taxa. Although the actual opsin is not known in Tridacna , it may be homologous to scallop Go opsin which also produces hyperpolarizing responses , placing it in the Group 4 peropsin clade Porter et al.
As noted above, functional studies of UV visual pigments are currently quite limited outside of the vertebrates and arthropods. Ultraviolet opsins. A Phylogeny of metazoan opsin sequences based on Porter et al. Clades are colored to reflect the four major groups of opsins.
C Evolutionary history of UV visual opsins in vertebrates and arthropods. Gray branches indicate groups with unknown sensitivity. Examples of photoreceptor spectral sensitivities involved in animal color vision systems. The UV range is shaded gray.
Some spectra A—E,J are inferred based on visual pigment absorbance and lens and ocular media transmittance. The thrips spectral sensitivity J is inferred from behavioral response.
All others are confirmed by direct electrophysiological measurements. Panels with multiple species use alternative colors, indicated on the plot.
See text for additional information. A Mammalian cones: mouse, Mus musculus Sun et al. B Avian cones: blue tit, Cyanistes caeruleus Hart et al. C Reptilian cones: Anolis cristatellus Loew et al. D Amphibian cones: poison dart frog, Dendrobates pumilio Siddiqi et al. E Fish cones: goldfish, Carassius auratus Bowmaker et al.
F Molluscan photoreceptors from giant clam, Tridacna maxima mantle eyes Wilkens, G Jumping spider: Habronattus pyrrithrix principal eyes Zurek et al. H Bumblebee: Bombus terrestris Skorupski et al. I Butterfly: Papilio xuthus Arikawa et al.
J Thrips, Caliothrips phaseoli Mazza et al. It is assumed that the thrips also has a green receptor dashed line , but this has not been confirmed. L Mantis shrimp: Neogonodactylus oerstedii Bok et al. Upon examining the evolution and spectral tuning of various UV opsins, some interesting trends emerge. Amazingly, often only a single residue is involved Shi et al. Furthermore, this dominant tuning site occurs at roughly the same location in transmembrane helix II across disparate opsin clades, at the residues homologous to position 86 or 90 in bovine rhodopsin Fig.
Positively charged residues in the binding pocket at these positions deprotonate the Schiff base Babu et al. Among vertebrates, SWS1 opsin is present in all major extant groups except elasmobranchs, including early-branching lampreys, where it forms a UV visual pigment Collin et al. Tetrapod SWS1 pigments, however, apparently shifted from UV into violet or blue sensitivity independently on multiple occasions in each lineage Yokoyama et al.
It is possible that the common reptilian ancestor of birds had a violet SWS1, but that some avian groups re-evolved UV sensitivity, often through the alternative tuning site at position 90 Hunt et al.
By contrast, the recent discovery of a UVS cone type in the emu, a paleognath bird basal in avian evolution Hart et al. It should be noted that, with the exception of teleosts, vertebrates typically only possess one copy of SWS1, making the tuning of this opsin sequence critical in spectrally mediated visual tasks. Chelicerate and crustacean SWS opsins always seem to form UV visual pigments, but in insects, one duplicated SWS clade has become blue- or violet-absorbing primarily by mutation of tuning site This is perhaps in compensation for the previous loss of middle-wavelength-sensitive MWS opsins in insects Henze and Oakley, ; M.
Bok, The physiological, ecological, and evolutionary basis of polychromatic ultraviolet sensitivity in stomatopod crustaceans, PhD thesis, University of Maryland Baltimore County, Although most animals with UV sensitivity possess only a single UV receptor type incorporated into a tri- or tetrachromatic color visual system, there are some notable exceptions. The situation in dipterans is further complicated by the frequent presence of a sensitizing pigment in the photoreceptor membranes that absorbs light strongly in the UV and transfers that energy to the visual pigment, adding a second UV sensitivity peak to longer wavelength visual pigments or augmenting the sensitivity of UV visual pigments Hardie and Kirschfeld, ; Kirschfeld et al.
The significance of multiple UV receptors in flies is unknown. Additionally, although the purpose of UV-filtering pigments in the lenses or ocular media of eyes is often to attenuate UV light falling on the retina, there are a few notable cases of spectral tuning and even the production of multiple receptor sensitivity types within the UV range by filtering.
However, the true champions of spectral expansion and photoreceptor tuning in the UV and throughout the entire visible spectrum are the mantis shrimps. Furthermore, one of these photoreceptor types is also sensitive to the polarization of UV light see Glossary; Kleinlogel and Marshall, The UV-filtering pigments are mycosporine-like amino acids, used by other animals as sunscreens or ocular filters to remove UV light, not to shape its spectrum Bok et al.
Chromatic aberration arises from a property that essentially all transparent materials such as those used in biological optics possess — their refractive index see Glossary decreases with wavelength.
Consequently, short-wavelength images are focused closer to a lens than longer-wavelength ones. Because UV has unusually short wavelengths, its focal plane lies well in front of those of visible wavelengths, thus blurring the image and decreasing its contrast. The effect of chromatic aberration increases with eye size, so one might expect only animals with small eyes to tolerate it and thus to be UV sensitive.
This is generally true, but as we show here, the exceptions are numerous. Given the optics of chromatic aberration, one possible way to manage it is to place UV photoreceptors closer to the lens than longer-wavelength classes. Invertebrates are generally small animals, and those that have compound eyes are essentially immune to the effects of chromatic aberration because the entire length of the photoreceptor acts as a single light guide, and resolution depends only on the separation of independent units.
Nevertheless, the UV receptors are almost always found closer to the lens than other receptor types. Here, however, the reason is to boost their sensitivity, not to cope with aberrations. Because all visual pigments absorb fairly well in the UV, placing UV receptors deeper in the retina would put them at the mercy of the overlying receptors, greatly diminishing number of the UV photons that actually reach them.
Still, there are invertebrates with multiple spectral receptor types and single-lens optics. Where these species have been carefully described, they generally do manage chromatic aberration by layering UV receptor classes at the top of the retina and also the longest-wavelength receptors in the bottom layers. Jumping spiders have large-lensed principal eyes, and their retinal tiers are nicely spaced to correct the chromatic aberration of the lens; the UV receptors are on top and the green receptors are lower — both at the correct focal plane for light to which they most strongly respond Blest et al.
As an aside, jumping spiders use focal plane changes to judge distance, but this apparently involves only green-sensitive receptors, not the UV system Nagata et al.
Of the relatively small number of other single-lensed, imaging invertebrate eyes that have been well characterized, only those of larvae of the diving beetle Thermonectes marmoratus definitely contain UV photoreceptors. Here, however, the UV receptors lie deeper in the retina than the middle-wavelength class, where they would be both shielded by the overlying retina and well behind the proper focal plane Maksimovic et al. This counterintuitive arrangement has yet to be explained. Vertebrates have simple eyes, and nearly always large ones.
Consequently, many species with UV photoreceptors potentially face chromatic aberration difficulties. In aquatic species, UV photosensitivity is mainly correlated with habitat, not with eye size. The largest fish eyes occur in high-speed predators such as tuna, swordfish or other billfishes; because these hunt away from the surface of the sea, the UV flux they experience is not strong, and they tend to be dichromats with blue and green receptor types. The lenses of most billfishes, in fact, block the entry of UV light into the eye Fritsches et al.
Amphibians tend to be small animals with rather poor spatial resolution, so they need not bother with correcting for chromatic issues. Most terrestrial animals, however, live in a world drenched with UV photons. If they have large eyes, they must face the issues caused by chromatic defocus.
The corresponding opsins vary at a single critical amino acid residue Wilkie et al. A potential solution to the chromatic aberration challenge that UV sensitivity imposes is the use of multifocal lenses in many avian species Lind et al.
Such lenses have the ability to focus both short- and medium-wavelength images simultaneously. Another solution is to remove UV light by filtering it out. A comprehensive study of ocular media among birds did show decreasing UV transmittance with increasing eye size, a finding consistent with controlling chromatic aberration at very short wavelengths Lind et al.
This same study found that raptors have among the least UV-transmissive eyes of all birds, which strongly suggests that their eye designs provide very high acuity without the contamination of out-of-focus light on the retina. Turning to terrestrial mammals, we already know from earlier sections that human lenses block UV entry very effectively. What about other species? Until recently, it was assumed that larger mammals were generally similar to humans, using yellow lenses to block UV. Marine mammals lack even blue-sensitive cones much less UV types , although this is not an adaptation for chromatic aberration Peichl et al.
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