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The evolution of vision

Clinical
Dr Douglas Clarkson considers the evolutionary processes behind the diverse vision systems across current and extinct species

Figure 1: Lithograph of Charles Robert Darwin, aged 40, in 1849, by Thomas Herbert Maguire. Image: Wellcome collection

Since vision plays such an important part in everyday living, it is relevant to reflect on the evolutionary processes involved. The area of vision system evolution has been of particular fascination for a wide range of scientists – especially biologists, zoologists, geneticists and palaeontologists – and where an extensive literature is available on the subject, including the diverse vision systems developed across current and extinct species.1,2

In the expansive world of the biologist, the human eye is merely a single detail within a diverse lineage of sighted species. The picture emerging of the evolution of vision, however, is by no means static as new fossil evidence emerges and the genomes of species of interest are decoded to establish evolutionary trajectories.

 

Dialogues with Darwin

It is always rewarding to access the original comments of Charles Darwin regarding the evolution of the human eye in his major work The Origin of Species.3 A key inspiration of this work, published in 1859, was his five year voyage on the survey ship the Beagle, which returned to England in 1836.

While Darwin acknowledged the marvels of a highly developed vision system, he at the same time expressed no doubt that given time the process of evolution could create such ‘organs of extreme perfection’. Darwin, however, was minded to indicate that a ‘process of extermination’ had removed vast numbers of pre-existing species coupled with the ‘extreme imperfection of the geological record’.

The publication of The Origin of Species launched an in-depth study of evolutionary biology to track the lines of evolution of vision within diverse species and which currently continues with the utilisation of much more advanced lines of investigation.

Darwin, however, was also aware of various clues regarding evolutionary trajectories including embryo development as indicated by his comment: ‘Thus the embryo comes to be left as a sort of picture, preserved by nature, of the ancient and less modified condition of each animal.’

Lamb, in more recent times, describes the metamorphosis of the larval eye of the lamprey into an adult over a period of five years as a clue to its evolutionary history.4

 

Unravelling a Mystery: the Origin of Photoreceptors

A key component of the molecular reaction chain to enable photon detection are the opsins, which present as complex families of G-protein-coupled receptors. The opsins are typically made light sensitive by the chromophore retinal. Within vertebrates this function is provided by so called c-opsins, which are stored in a stack of disc-like surfaces.

Within the group of species known as protosomses as a division of so called bilaterians (species with two-sided symmetry), which include insects, worms and squid, this function is undertaken by r-opsins, which are part of a different sequence of pathway signalling for photon detection.

These differences had suggested the vertebrates and protosomes developed their respective opsins after an evolutionary divergence of the two groups. The detection of c-opsins in the ragworm by Arendt et al, however, implied the common ancestor of protosomes and vertebrates already had both types of opsin.5

Jellyfish, as part of the cnidarian group of species which include also sea anemone and corals, had always been considered significantly different from bilaterians due mainly to the lack of a developed nervous system. This had in turn implied that such groups had developed eyes independently.

The discovery, however, that the genome of Hydra magnipapillata a cnidarian freshwater polyp contained genes for opsins6 indicated that opsins had evolved much earlier than bilaterians. It is likely that cnidarians and bilaterians diverged around 620 million years ago (Mya) and that both groups subsequently had the potential to utilise both types of opsins in photodetector systems.

It is likely also that both sets of opsins emerged earlier than this date from a single opsin type. In the evolutionary scale of significance, this event was a precursor of refinement of photoreceptor development in countless subsequent species. Early forms of life could have used such photoreceptors as light detecting systems to provide a measure of phototaxis, posture control and regulation of depth in the ocean.

Looking back further in time, melatonin is a receptor protein that could have been the precursor of the family of opsins. During darkness melatonin rises in level across almost all species7 and is oxidised by daylight so an organism able to detect levels of melatonin could derive an awareness of night and day, though melatonin is required to be produced on a continual basis to achieve this.

The opsin pathway provides, however, a much more convenient mechanism, which can be continuously used and
re-activated. Verasztó recently described the role of c-opsin and r-opsin photoreceptors to form a spectral depth gauge in marine zooplankton where the ciliary photoreceptors are sensitive to ultraviolet light and the rhabdomeric photosensors sensitive to visible light.8

It is conjectured that feedback from the two sensors allow the zooplankton to avoid high levels of harmful ultraviolet light but receive sufficient visible light for synthesis of organic matter from water and inorganic nutrients. A key development of vision systems was the emergence of devices for more efficient detection of light where discrete units of light detection were derived from stacked layers of photoreceptors to increase the likelihood of photon detection.

Two ways of stacking such membranes were developed as micro villi with r-opsin (rhabdomeric photoreceptors) and modified cillia (ciliary photoreceptors) with c-opsin. This development currently exists throughout the animal kingdom and indicates two key evolutionary milestones in the development of the photoreceptor. The development of a more sensitive photoreceptor was a key stage in the further development of more useful visual function.

 

Evolutionary Outliers

Eyes tend to develop where there is pressure from competing species or where there is a requirement to find sources of food. Lamb et al describes the eye of the current day hagfish, which contains basic elements of primitive early vision systems and where the creature retains a light sensitive spot but no formal eye.4 The hagfish survives by feeding on fish that fall to the ocean floor and where a key survival activity is to emit slime that chokes the gills of an attacking species.

They are mostly found at depths of between 200 and 1,000 metres. Able to survive in its specific environment, there has been no evolutionary advantage to develop a more highly developed vision system. Instead, they have developed highly sensitive olfactory senses to detect their prey.

 

The Cambrian Explosion

Towards the end of the Precambrian era hardly any fossils exist as evidence of the life forms that then were present. Then within a period as short as five million years, the so called ‘ Cambrian explosion’ occurs around 540 Mya. Evidence of this was initially found by palaeontologist Charles Walcott in 1909 in the 515 Mya rocks of the Burgess shale9 in Canada.

The interpretation of the Burgess shale has been significantly assisted by more recent fossil discoveries of this period. In 2019, a stunning discovery came to light in the Hubei province of China10 of soft bodied species including jellyfish and sponges preserved by a mudslide from 518 Mya. Previously a smaller but significant discovery from 519 Mya in Yunnan in China provided information of the eyes the arthropod Isoxys.11

This creature is estimated to have been about 2.5cm in length and where evidence was obtained of a pair of compound eyes utilising small spherical lenses as outlined in figure 2 (pictured top right). This would have allowed the creature to successfully forage for food but perhaps not provide warning of approaching predators. Figure 3 (middle right) indicates a fossil trilobite specimen where the structure of the compound eyes have been preserved and which could vary in number from a few dozen to many thousand.

Trilobites are thought to have emerged around 521 Mya shortly after the beginning of the Cambrian period and survived for around 300 million years. A larger creature of the Cambrian period such as Anomalocaris (figure 4, pictured below, right) is understood to have had a pair of compound eyes about several centimetres in diameter, which it used to hunt its prey.

It is likely that the trigger for creation of wholly new types of species within the Cambrian explosion was the development of improved visual systems that yielded highly significant advantages in terms of predatory activity and associated defensive strategies. The compound eye appears to have been more easily developed at this stage than eyes with a single lens. The emergence of vision systems across the Cambrian explosion and beyond is usefully summarised by Schwab.12

 

Emergence of Eye Shapes

If, however, an essentially flat layer of photoreceptors assumes more of a cup shape, then this marks the beginning of being able to obtain more information from the detected light. The pattern of light on the photoreceptors will change, for example as a potential predator approaches. Such consideration is based on aquatic species and where the developing cup recess is initially water filled.

While this early line of development was taking place, many species opted for the development of compound eyes, where each ‘mini cup’ was linked to a dedicated photoreceptor and which remains the vision system of choice for countless species today. While such compound eyes provided essentially equivalent solutions to basic vision, they probably were not the most efficient way of utilising available space for vision.

The basic rudimentary cup shape arrangement of photoreceptors remains a key component of vision in many aquatic species. Nilsson and Pegler estimated using a computer simulation that the phase of transitioning from an eyespot with light sensitive cells on the surface to an organism with a rudimentary camera/lens style eye could take place in around 364,000 generations or around a million years.13

A reason why such changes could happen so rapidly was the tremendous advantage provided by improved vision. In some ways this event depicts the general process of evolution as a process with ‘blips’ of significantly heightened activity. Nilsson indicates in figure 5 (right) one of the several eyes of the unique but dangerous box jellyfish, which indicates an array of photoreceptors, spherical lens and protective cornea.14

The acquired vision provides the unique ability to hunt prey by self navigation and maintain its location close to mangrove swamps. It is a surprising fact that box jellyfish kill many more people each year than sharks. The requirement to detect changes in light field across the array of photoreceptors required the photoreceptors to be able to respond more rapidly.

Modern methods of simulation of the sensitivity of basic cup detectors using ray tracing indicate the limited sensitivity range of such systems and where the inclusion of a lens of transparent material extends the usefulness of such a detection system, though as yet it is not capable of capturing useful images. With increase in eye size and refinement of lens function, the system becomes capable of image capture.

In this process of eye evolution the process of lens development varies considerably between species based on the availability of materials. In general the transition from aquatic species to terrestrial species resulted in the flattening of typically spherical lenses due to the additional refractive power of the air/cornea interface. This trend has recently been confirmed by micro x-ray CT scanning of preserved specimens of frogs and toads.15

The eye of the present day nautilus is based on a water filled spherical eye shape without a lens and with an open aperture as a means of light entry (figure 6, right). The light levels at its maximum depth of around 500 metres, however, would not support any meaningful vision. It is likely that the evolution of this eye did not progress to include the inclusion of a lens because of the development instead of its olfactory senses. This species, whose design remain essentially unchanged as a ‘living fossil’ from 500 Mya, is described by John Fortey in his award winning book ‘Survivors’.16

 

Classes of Photoreceptor Behaviours

Nilsson provides a useful classification of vision in species derived on a functional basis as indicated in table 1.17 In class I of non-directional behaviour, the basic vision system detects the presence or absence of light and can provide the input into a circadian clock. Class II provides for an element of directional photodetection allowing an organism to head towards the light or conversely avoid it.

Class III provides for low-resolution vision that can be used to detect self motion, locate suitable habitat and detect motion of objects into the visual field. Class IV provides for high-resolution vision, which allows detection of food sources, warning of predators and communication with other animals. Between each stage there is a significant increase in the level of information required to be processed.

The track of evolution from Class I to various levels within Class IV can be identified as a progression through the various stages. It is possible, also, to find existing species at every stage within the various classes. The move towards Class III and IV is associated with increased sensitivity of photoreceptors based on stacking of photoreceptor membrane layers. Also, the speed of response of photoreceptors is correspondingly increased sufficiently to respond to moving objects.

In terms of factors driving evolution of vision, a key element is identified by Nilsson as visually guided behaviour where such a factor directs the development of visual organs.

 

Evolution of the Vertebrate Eye and Beyond

It is only with novel fossil discoveries and the development of improved techniques of their structural investigation of acid etching and x-ray CT as described by Young that valuable insight has been obtained regarding the early development of the vertebrate eye.18 A specific example is described of Murrindalaspis fossil fish from lower Devonian limestones in New South Wales, Australia from 400 Mya where a combination of techniques identifies structures of sclerotic ring enclosing the eye, the optic nerve, optic artery and vein and groups of eye muscle scars.

By around this time 400 Mya the vertebrate eye had largely developed into its general structure evident today. One theory regarding the subsequent evolutionary ascent of mammals19 is that during the era of the dinosaurs, the originating species was forced into a nocturnal lifestyle and which changed the evolutionary demands of their vision systems. With the disappearance of the dinosaurs around 65 Mya, the prototype mammals could again survive in a daylight world.

It is considered that the fovea first appeared in evolution in the temporal retina of fishes. It subsequently evolved in birds, disappeared in primitive mammals, though reappeared in primates. The development of the fovea has been a key asset in human development and activity. A useful observation of Hendrickson, however, is that at birth the human fovea has less than 20% of the cone density of the adult and may be more susceptible to adverse influences during the period of early post-natal development than other primates.20

Of Rods and Cones

From an evolutionary perspective it is apparent that the importance of rod photoreceptors in human vision as a key element of species survival is diminished in modern life since a much greater extent of time is spent in light levels where rods are not able to function. Rod enabled vision as described by Lamb was specifically developed to detect low levels of light and where rods are responsive to single photon events.21

A key enabling facility of this is the ability of the rod bipolar cell to act in ‘threshold’ mode and disregard photoreceptor dark noise. A key adaption is also to use of a common output channel for local rods and cones. The transitioning from light conditions to dark conditions, however, can take up to 40 minutes to achieve maximum sensitivity. Cone cells only make up around 5% of the total number of photoreceptors in the retina.

Anderson et al have described how the low spatial acuity of peripheral cone mediated vision is a result not of low density of cones but related to the pooling of retinal ganglion cells.22 Such pooling effects are in fact greater for rod vision. Where excellent night vision is a key species requirement, this can be provided by increased rod density and also the inclusion of a reflective layer behind the retina – the tapetum lucidum – to increase the likelihood of photon capture.

From an evolutionary perspective, it is considered that the single photon detection by rod photoreceptors came into being between 400 to 500 Mya as a variant of existing cone type photoreceptors. By using predominantly rod-based photoreceptors, this optimised the ability to see in exceedingly low light levels and enabled, for example, marine species to extend to the ocean depths.

Before the advent of genomic determinations of species, heralded by the determination of the first human genome in 2003, the actual mechanisms driving changes in vision systems in species was unknown. With the subsequent mapping of genes in species responsible for vision systems,23 a clearer understanding of such highly complex mechanisms has been obtained with the suggestion that the genetic apparatus to develop eyes was established at a much earlier time in the evolution of species than was previously thought.

 

Evolutionary Complaints

Ophthalmologists have been known to comment on the degree of perceived imperfection of the human eye24 and comment on issues such as the inversion of retinal photoreceptors, which degrades light detection and increases the likelihood of retinal detachments. Various theories have been proposed regarding the inversion issue, which involve complex issues relating to the metabolism of photoreceptors, so an automatic assumption that this was an evolutionary error may be over-hasty. The perspective provided by the evolution of vision, however, is identified by de Sousa as a mechanism for identification of useful lines of present day research.25

 

Summary

The research into the function of vision of diverse species is ongoing and where clues relating to the evolutionary changes that they provide continue to refine the related evolutionary road map. This research, however, overlaps into a great number of scientific disciplines, which tend to function within their own spheres of interest. It is paradoxical, however, that this is taking place at the start of a period of mass extinction of species where the rate of loss of species is considered to be between 100 and 1000 times greater than ‘normal times’. 

  • Douglas Clarkson is research fellow in Department of Clinical Physics and Bioengineering at UHCW NHS Trust, Coventry.

 

References

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