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To explain the Blog

Life first emerged approximately 3.75 billion years ago from the swirling broth of the prebiotic soup. The process leading to its appearance is only partially understood, but has several possibilities. The harsh conditions on earth at the time would have permitted only an organism capable of withstanding such bleak surroundings.  It would have been very different from any alive today. Survival of any life form in that environment would have required analysis and interaction with its birthplace habitat, skills that would require sensory abilities.  Such sensory understanding would have been essential for, and crucial to, life’s evolution.

Sight is but one member of a family of sensory abilities, yet for most creatures it is a dominant and pivotal one. But sight is probably not the first sense acquired by those early cells, nor were the necessary components of vision secured for the purpose of sight.  As often occurs, evolution co-opted various molecules that were assembled for other purposes. These changes and biochemical redirection leave traces suggesting the path of early photoreception.

The witness and progress of photoreception is a fascinating window on evolution with a perspective unlike any other because it includes eyes.  We will review what is known about the evolution of photoreception and the development of vision, not necessarily in chronological order, but rather in an order that illustrates the goal in conjunction with the progress. Along the way, we will comment on and discuss cutting edge research currently ongoing across the world.

This is the story of how eyes evolved.

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Amazing Four-eyed fish

       Most animals have evolved eyes that focus in air or in water. Some have evolved eyes to have an aerial or aquatic view at different times, but few species indeed have evolved a design that can focus in both media simultaneously.  Anableps anableps does just that.

       “Cuatro Ojos,” as the fish is known in Brazil, seems to be so odd as to be unbelievable.  But, these incredible fish, and their close relatives, have evolved the necessary adaptations to prosper as intertidal specialists, and can be found in fresh, brackish, or even pelagic waters.

        There are three different species of Anableps and while the ecology of the three differ somewhat, each has similar environmental needs for multiple eyes with similar ocular design. All three species grow to a maximum of 30-35 cm and resemble flat, floating cigars with large eyes with the long axis of the body of the fish parallel to the surface of the water.

All of these fish can see simultaneously in air and water using a unique ocular design as can be seen in the figures.  The aerial cornea is steeper and the pupil larger than the aquatic counterpart. The iris displays a finger-like projection that divides the pupillary aperture into two halves and corresponds to the pigmented band on the cornea. The iris and corneal ridge create a separate pupillary aperture for both the aerial and the aquatic images.  When dilated, the two separate pupils form a single, dumbbell-shaped aperture.

The lens is oval, pyriform (pear-shaped) and asymmetric with the more rounded, circular portion of the lens found in the ventral half of the eye corresponding to the aquatic portion of the globe, and the flatter portion of the lens dorsally corresponding to the aerial pupillary axis (Figures 1&2).  As a result the lens diameter is smaller along the aerial visual axis as compared to the aquatic axis(1) .  The lens is oval in equatorial cross section, instead of round, and has the accommodative mechanisms of anterior-posterior movement along the visual axis of the pupil as do other fish species.

The inner nuclear layer of the retina (cells that help process the image) in the ventral half of the globe, subserving the aerial field, is thicker and contains more bipolar cells as compared to the dorsal half. There are more ganglion cells in the ventral retina, with perhaps one-half to two-thirds as many in the dorsal half of the retina.  The retinae are distinct in that there is a separation between the two halves that subserves the aquatic image as compared to the inferiorly positioned retina that subserves the aerial image. There is a single optic nerve that receives projections from each separate retina.

The optical structures in Anableps allow simultaneous vision in the air and water by having two different optical axes in the same eye.  Projections of  the nerves of both the aerial and aquatic visual fields has been mapped by electrophysiologic methods (to the visual tectum). Interestingly, the visual fields have been found to be similar to that of other freshwater fishes except for a horizontal band above and parallel to the water line with a greatly enlarged tectal (area of the brain) magnification which correlates with the increased ganglion cell density in the ventral retina.  The threshold for movement is lower in the aerial visual field than in the aquatic field and seems correlated with a much higher cone density in the ventral as compared to the dorsal retina. The retina consists of rods, single cones and two different classes of double cones.  The cones have visual pigments with maximum absorbances of 409 nm,463nm and 576nm respectively.  Clear oil droplets, which are better termed ellipsosomes, are noted in the inner segment of some of the cones(2).

Evolutionarily speaking, the Anableps species are neither primitive nor particularly advanced. This small specialized family of toothcarps, Anablepidae, contains only three species, A. anableps, (mainly brackish– eastern South America) A. microlepis (North and northeast coast brackish and oceanic—eastern South America), and A. dowi (Pacific coast, Central America).  All three species, but especially A. dowi, eat insects above and below the water line.  A. dowi is even an active nocturnal hunter pursuing prey on mud flats out of water. These fish feed above the water surface, at the water surface, and in the water column.  They leap out of the water to attack aerial insects and use their aerial vision for this purpose.  All three, but especially A. anableps and A. microlepis, feed on the tidal flats sifting through the mud with unusual teeth acting as a sieve.  The aerial vision with the superior cornea and superior half of the lens provides for excellent acuity and can be used to locate prey, but is especially used to alert the species to predators.  Birds and small aquatic predators are the danger, although most aquatic predators will not follow the species into the tidal flats. Since Anableps has no lids, it will frequently submerge the aerial eye to wet the surface, and, if on dry land, to wet its gills.  All three species probably rely on their aerial vision for protection against predators as a primary function, and feeding tends to play a somewhat less important role.

In the three Anableps species, we have an animal that occupies a specialized niche requiring excellent aerial vision for feeding and especially for protection against predators.  These fish certainly illustrate that double vision may have its advantages.

 

(1)       Schwab I:  Tr Am Ophth Soc. 2001; 99:145-57

(2)       Avery JA: Nature 1982; 298,62-63

Figure 1 Anableps at water level with one eye above water

Figure 1 Anableps at water level with one eye above water

Figure 2  Anableps viewed from above

Figure 2 Anableps viewed from above

 

Figure 3 Anableps viewed from below water line

Figure 3 Anableps viewed from below water line

Figure 4 Histologic section of aerial portion of globe.

Figure 4 Histologic section of aerial portion of globe.

 

 

 

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Jumping spiders and their magnificent eyes

Most spiders get a bad rap. Few would harm you, and only rarely are spiders aggressive towards humans.  Most will defend themselves if threatened,  of course, and a few are venomous. Most spiders, however, would prefer to ignore humans and be ignored by us. A few species are curious, quite interesting and most appealing.  Jumping spiders, for example., reveal visual mechanisms unknown in the rest of Animalia.

Jumping spiders are positively charming creatures, and you will know that to be true if you have ever watched one closely.  These are common spiders and range from approximately 3 to 17 mm in length and will watch you closely as you approach them.  They have four pairs of eyes, with the large anterior median (AM) set the most obvious (Figure 1). These circular eyes provide an “attentive child” appearance because they are fixed and are relatively large based on body size, but are tiny on an absolute scale.  These placid eyes belie the organized complexity and evolutionary genius that lies beneath the carapace.

The AM eyes are Galilean telescopes with a corneal lens fixed to the carapace, and a second “lens” at the end of a small tube immediately in front of the retina. This second lens deserves a closer inspection.  It consists of a steeply sloped pit at the retinal level (Figure 2). This pit is analogous to our fovea, or area of sharpest vision. There is an index of refraction gradient between the amorphous fluid in the tube (analogous to vitreous in the center of our eye) and the wall of the foveal-like pit. The tissue lining the pit is the retina.  This pit and the index of refraction gradient create a minus lens and a Galilean telescope, much like the fovea of many raptorial birds. A creature this small cannot have much retinal area, so to maximize the number of photoreceptors struck by photons, the retina is tiered. This means that there are 4 layers of retinal cells for light to traverse.  Each layer of retina extracts information from the light passing through the photoreceptive portion of the cell, called a rhabdom, into the next tier until it strikes the fourth and final layer. The angle of separation from the center of one rhabdom to another perpendicular to incident light is approximately 1.7 micron, creating a mosaic slightly more than three times the wavelength of visible light rays.

This visual system is indeed unique and begins with the aforementioned corneal lens connected to an elongated tube within the cephalothorax (first segment of the spiders body).  There are six muscles to move the tube.  Since the external cornea/lens is fixed to the carapace, it creates an image that is fixed at one point within the tube.  This compact telephoto lens system combined with the tiered retina achieves excellent acuity, but only a very tiny field of vision. So, to increase this field of acute vision, this optical marvel moves the tube housing the retina with six muscles per eye by mostly scanning movements. This is akin to a raster scan similar to those seen on a TV or computer screen.  Jumping spiders scan their world much like painting a wall with a fine brush although the retina is not linear, but shaped more like a boomerang. The other pairs of eyes do not scan and are principally used as motion detectors to find other animals for the AM eyes to decipher.

With the AM eyes, jumping spiders have the finest discrimination of all arthropods, and probably all invertebrates as they are visual hunters, whereas most other spiders use the tools of silk.

There is more to this story, though, as recent work by Nagata has shown. Focusing on a prey item would be key to the success of any visual predator. Jumping spiders cannot focus as easily as most vertebrates because they cannot accommodate, or change the shape of their lenses as most vertebrates do. Furthermore, they do not have stereopsis as humans do because the field of view does not overlap as it does in humans or other animals that have stereopsis. Some few insects, and, vertebrates to some extent, can also tell distance and a form of focusing by parallax when the prey item or the predator moves. The mental gymnastics of distance measurement of a telephone pole seen from a moving car window as compared to the scene behind it is an example of such motion parallax.  Jumping spiders cannot accommodate and cannot move their eyes. If the spider moves, it may frighten the prey, so the spider needs another mechanism.  Nagata and his fellow investigators have shown that jumping spiders use defocused green light from the third of the four layers of visual pigments mentioned above and compare it to green light that is properly focused on the visual pigment in the layer directly beneath that third layer.  In some ways, this would resemble parallax but would be a quite different, and very clever, mechanism.

Evolution has found a simple, elegant to measure distance using only color. This permits this tiny eye to be an excellent visual instrument especially at short distances, with surprisingly good acuity that is far better than any compound eye found in other arthropods.

Land M: J Exp Biol 1969;51:443-70 &  J Exp. Biol 1969;51:471-93.

Harland, D.P. Jackson RR (2004) pp. 5-40. In: Complex Worlds from Simpler Nervous Systems (F.R. Prete, ed.). MIT Press, Cambridge, Massachusetts.

Nagata R, Koyanagi M, Tsukamoto H, et al:  Depth perception from image defocus in a jumping spider. Science 2012;335: 469-471.

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The Eyes of Anomalocaris

The lord and master of the Cambrian seas was the undulating predator Anomalocaris. It was likely highly efficient, and now we are learning, highly visual. It was considerably larger than any other creature in those shallow seas and must have evoked fear with nothing more than its shadow.

Carnivory and predation were two key elements ushering in evolution and this generally requires vision as a principal sensory input. Sure enough, Anomalocaris had two eyes on stalks probably giving it a wide visual field. But, until recently, we have known very little about its visual capabilities and mechanisms. That has changed.

In a well-considered manuscript, Paterson et al describes fossils of the eye of Anomalocaris. From this work we now know that that this magnificent animal, probably the first in the line of apex predators of these shallow seas, had a compound eye that, in many ways, resembled the eye of today’s dragonfly.  Anomalocaris had perhaps as many as 16,000 hexagonal facets (individual units of the eye called ommatidia) in each eye and probably good vision. For reference, extant dragonflies have approximately 25,000 ommatidia and surprisingly good vision. Although I doubt that this Anomalocaris had vision good to read the newspaper, its vision would have been very good, at least in bright light. Its compound eyes were likely of the simplest and most common design—the apposition compound eye. This eye would require a great deal of light, and restrict the animal to a diurnal lifestyle. It would have been restricted to the rather bright light environments such as those found in a coral reef of today.  Almost certainly Anomalocaris would have had a wide field of vision and surprisingly sharp vision for smaller prey—just like a dragonfly.

With its anterior “arms” for capture and its mouth located beneath the proximal portion of its body, this first top predator would have had few competitors. Its prey species were soft bodied as it was as well. Such predation would inevitably drive the predator-prey “arms race” and could well have been instrumental as the stimulus for the evolution of hard shell-like bodies.

With Permission of the Royal Ontario Museum and Parks Canada © ROM-Photo Credit: J.B. Caron.

Paterson JR, Barcia-Bellido DC, Lee, MSY, et al:  Acute vision in the giant Cambrian predator Anomalocaris and the origin of compound eyes. Nature 2011; 480:  237-240.

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Solar panel wasp

 

Oriental Hornet (Vespa orientalis)

Photosynthesis is usually the province of the plants. Very few animals can actually make energy from sunlight. But, some few members of the animal kingdom have harnessed the sun by getting the necessary solar panels to “go green.”

An ancient process, photosynthesis began between 3.75 to 3 billion years ago in single-celled organisms likely related to cyanobacteria. This process uses the sun’s energy to convert carbon dioxide to compounds such as sugars that are capable of producing energy for the cell. As cells evolved and became more complex, these photon-loving bacteria (cells without a nucleus also called prokaryotes) were then incorporated into the evolving cells as plastids and used as energy sources. Eventually, these single-celled eukaryotes (cells with a nucleus that are more complex than prokaryotes) would radiate into plants and would rely on photosynthesis for billions of years. Animalia, however, has not pursued this path. Instead, the animal kingdom has used ATP to provide the necessary energy for life.

But, a few animals have re-established photosynthesis as an energy mechanism, indicating either that the potential for this system remained with the more complex animals, or more likely, that these animals developed this energy powerhouse on their own in a bizarre example of convergent evolution.

The oriental hornet (Vespa orientalis) has evolved yellow patches located on the dorsal surface of the abdomen that Plotkin et al (Plotkin M et al: Solar energy harvesting in the epicuticle of the oriental hornet (Vespa orientalis) Naturwissenschaften (2010) 97:1067–1076) have shown are photosynthetic or at least harvest light as an energy source. In a competitive world, the extra energy obtained from this photosynthetic patch creates a successful edge. As a bonus, it permits this wasp to be active during mid-day with the maximum output of photons when other wasps are not so active.

Extraocular photoreception is found in many if not most creatures, but perhaps this extra light is never used so prudently as it is in the oriental wasp.

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Cryptochromes

Cryptochromes

Rhodopsin is a photoreceptive molecule composed of a Vitamin A derivative (retinal) and an opsin. Opsins are proteins that complement the retinal, and are “tuned” to certain wavelengths of light, and this means that they respond most vigorously to a certain wavelength but usually respond to wavelengths close to the critical wavelength.  Opsins can be identified as being tuned to “green” but this is misleading as that opsin will have a peak response to wavelengths in the green range, but respond to light with longer and shorter wavelengths, too.

All metazoan opsins are related, making them homologous. They probably arose from a single opsin and have mutated or diverged.

Rhodopsins are the principal molecule that responds to light in animals, and creates the impulses that lead to sight, and most animals that have vision do so with a form or rhodopsin.

But, Vitamin A and an opsin are not the only way to receive and respond to light. There are other molecules that respond too, and some are important to vision in many animals.

The cryptochromes are biochemical molecules that respond best to blue light and are quite ancient. These probably arose from DNA repair molecules called photolyases, or at least the cryptochromes are close cousins to the photolyases. The DNA found in early and ancient life was easily damaged by ultraviolet light, and there would have been a lot of UV because there was no oxygen to make ozone, and few  other molecules in the atmosphere.  The DNA would found a way to be repaired, which would have been through the photolyases. These chemicals probably evolved into cryptochromes. Cryptochromes are derived from flavins or Vitamin B2 , and can convert the energy of light into chemical energy. This would have been a valuable asset to an early cell , and hence, this chemical would have been used in by almost all cells in some way.

Cryptochromes are responsive to blue light, and when these chemicals first arose, there was likely a lot of blue and ultraviolet light. Cryptochromes are able to use that energy to repair DNA. Cryptochromes are very common and present in almost all (if not all) plants, animals, and even many forms of bacteria. Most of the time, these molecules are used to set circadian rhythms or to measure light and dark. But, not always.

Cryptochromes are used by many corals especially in the southwestern Pacific to measure the length of moonlight and the color of the moonlight. This permits these corals to synchronize with each other to spawn on virtually the same night in early spring every year.

Why would corals want to spawn at the same time each year?  Predators like to eat the spawn (essentially eggs) of almost any animals including coral, but with so many eggs it is impossible for the predators to eat all of them The volume of release is simply too big. Furthermore, if the male and female spawn are released at the same time into the water, they stand a much greater chance of finding one another to spread the species. As it turns out, this is the largest mass sex act in nature.  All in one night!  Cryptochromes are important in other ways, and we will visit them again.

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Pterosaurs

These dramatic reptiles arose in the Triassic and continued a150 million-year sovereignty until the end of the Cretaceous. During this time they were uncontested champions of flight, and ruled the skies. Although often thought of as dinosaurs, they were but cousins to them. Sometimes incorrectly called pterodactyls (members of a specific genus within the pterosaurs, but not a synonym), pterosaurs were the first flying vertebrates and had a spread from wingtip to wingtip of about 16 cm to over 15 meters. The latter behemoth was Quetzalcoatlus northropi and was the largest creature to ever fly.  By comparison, the largest wingspan of a living bird, a wondering albatross, has been measured at a bit over 3.6 meters, less than one-quarter of the wing extent of this magnificent reptile.

Although we know little about the eyes, they were enormous and contained scleral ossicles (bones to support the structure of the eye) just like most reptiles. Many investigators believe they were warm-blooded, and probably had good if not excellent eyesight—just like birds. The pterosaur’s internal nutritional structures and retinal circuitry were likely very similar to those of modern birds, too. While most were likely diurnal predators, pterosaurs had likely had nocturnal lineages, as well.

The fossil braincases of these creatures have been examined and show enlarged floccular lobes. The flocculus is important in balance and flight and birds have similar enlargements. These measurements strongly suggest that the pterosaurs were highly skilled predators with accurate visual processing and spectacular flying abilities. Some of the largest of them probably weighed up to 65 kilograms, and must have had a daunting and frightening presence coming over any horizon.

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How a kingfisher hunts

Kingfishers

         True aquatic kingfishers are a generally secretive family (Alcedinidae) with dramatic feeding habits.  Most are brightly colored, often solitary fishers. They usually nest in banks along the riverine habitats in which they live.  A smaller number of kingfishers are terrestrial birds that are somewhat more social but still strictly carnivorous and usually found near water.  Both groups have exceptional vision, especially for their watery niche.

         Most aquatic kingfishers hunt by hovering above the water where their prey lives. They wait until the target fish appears in the proper position, and then they drop like a stone to pick the fish out of the water. The hunt is relatively brief, but thoroughly exciting to witness.

         Visually, they accomplish tasks that are nothing short of astonishing. Each of their two eyes has two foveae. The fovea is the area of an eye with the best vision because of the concentration of visual cells called photoreceptors. You use your fovea for best vision—for example, you are reading this sentence with your foveae. 

         Kingfishers have two foveae in each eye, with one fovea near the beak, and having the best vision by virtue of the highest concentration of photoreceptors. This is the fovea a kingfisher will use to sight its prey during the period of hover. During the drop to the water’s surface, the kingfisher sights the fish with this nasal fovea with the sharpest vision. But, once the kingfisher’s beak hits the water, the fish senses the vibration and shock wave coming from that beak entrance. The fish, being alarmed, may respond by trying to escape in an unpredictable manner, and if the kingfisher can’t react to that movement and direction, the hunt will be unsuccessful.

         By the time the kingfisher can determine the direction of the target fish, his eyes will be close to or in the water. This changes the angle of the incoming image because of the index of refraction of water.

         The kingfisher solves this problem with a second fovea in each eye. Once the eyes are immersed in water, the image of the fish is focused on the second fovea in each eye. That means that there is stereoscopic visualization of the prey as it tries to dart away, an action that is usually not successful.

         But, in order to keep the image focused on both foveae, the lens has to be oval and the second fovea has to be in the periphery of the eye at the edge of the retina.

         This unusual anatomic variant permits the kingfisher to be virtually unerring in its hunt. 

         Little work has been done to understand the optics of these eyes, but two images are attached below illustrating the two foveae and the asymmetrical lens. These are taken from an article referenced below.  Kolmer VW: Uber das Auge des Eisvogels (Alcedo attis attis). Arch f.d. ges. Physiol., Bd. 204,pp266-274. This is a most interesting arrangement and unlike that used by any other animal on earth.

Oval kingfisher lens in upper image and a cut section of the eye in the lower image.

 

Oval asymmetrical lens of kingfisher

 

 

Section of kingfisher eye showing where two foveae are located

 


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Oldest eye?

Metacanthina issoumourensis

For many years, the first confirmed eye was thought to be that of a trilobite, Olenellus. The eyes of trilobites fossilize easily because they are composed of a form of calcium carbonate, called calcite. (The white cliffs of Dover are composed of calcium carbonate.) Calcite is a crystalline form, which, under certain conditions, can form a clear lens that is perfectly able to focus light. Coincidentally, this crystal also fossilizes so well that sometimes such lenses can be used today even though they are hundreds of millions of years old.  Trilobites evolved the capability to make such lenses as the focusing portion of their eyes. When the trilobite fossilized, so did the eye, allowing us to document this eye, even knowing its refractive status.

This probably wasn’t the first eye because it is too evolved to have appeared de novo. Other less derived eyes likely appeared many times before this one. Since soft tissue does not fossilize well, often not at all, we don’t know as much about earlier eyes.

Recent reports from Kangaroo Island off the southern coast of Australia, however, provide definite evidence of an eye that was at least contemporary and perhaps older than that of Olenellus. It is derived enough that it could not have been the first eye either, but now it becomes one of the oldest known eyes, if not the oldest.

In a recent report in Nature by Lee et al (Lee, MSY, et al:  Modern optics in exceptionally preserved eyes of Early Cambrian arthropods from Australia. Nature 30 June 2011. 474; 631-634), a new candidate for the first eye, or at least a very early eye, is another arthropod. The creature was disarticulated and hence is known only from the eye, and may be from an animal already known though other fossils. Consequently, it is unnamed at present until more is known about its body.  Although the animal species is not known, the find appears to be a portion of the carapace discarded during ecdysis (shedding). If that is the case, the shed imprints of the eye resembles those of some extant insects or alternatively long-bodied decapods, such as a lobsters or shrimp.  It has a compound eye with perhaps 3000 ommatidia (the individual units of a compound eye, like a fly’s eye; it is derived from the Greek for “little eyes.”).  This animal, whatever it was, is an important step in understanding the evolutionary development of eyes. This newly discovered remnant of an eye is more derived and better organized than that of Olenellus although the Olenellus specimen is probably a bit older. Analysis of the multiple fragments of these specimens leads these investigators to believe the creature was a relatively fast-moving predator with binocular vision, capable of activity in dim light, including hunting.

Whatever animal is the source of this fossil, it is important and illustrates that eyes were probably well developed before the Cambrian and/or the speed of development of eyes was potentially quite rapid.