Eye (2018) 32, 302–313 © 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved 0950-222X/18 www.nature.com/eye RCOPHTH EPONYMOUS LECTURE The evolution of eyes: IR Schwab major steps. The Keeler lecture 2017: centenary of Keeler Ltd Abstract represent an early form, or more likely they are a direct descendent, of such ancient cells. The Ocular evolution is an immense topic, and I do oldest fossils of cyanobacteria can be found in notexpecttocoverallthedetailsofthis the form of stromatolites (Figure 1). The sun’s process in this manuscript. I will present some light, limited only by its physical properties, concepts about some of the major steps in the was, and is, the principal source of energy for evolutionary process to stimulate your thinking such cells. The very short wavelengths such as about this interesting and complex topic. X-rays and gamma rays create free radicals and In the prebiotic soup, vision was not would be damaging to cells. The longer inevitable. Eyes were not preordained. Nor wavelengths such as radio waves do not carry were their shapes, sizes, or current physiology. enough energy and are too large to permit much Sight is an evolutionary gift but it was not discrimination. The visible and nearly visible ineluctable. The existence of eyes is so basic to light from the near ultraviolet extending into the our profession that we often do not consider infrared, though, would be useful if this energy how and why vision appeared or evolved on could be captured without harm to the cell. earthatall.Althoughvisionisaprincipal These frequencies would be the sweet spot sensory modality for at least three major phyla providing sufficient energy yet small enough to and is present in three or four more phyla, permit good discrimination. To use the sun’s there are other sensory mechanisms that could light would require conversion of these critical have been and were occasionally selected wavelengths to energy to fuel cellular instead. Some animals rely on other sensory metabolism. mechanisms such as audition, echolocation, or A cyanobacterium was likely the first olfaction that are much more effective in their fi particular niche than would be vision. We may organism and probably became the rst 1,2 not believe those sensory mechanisms to be as chloroplast by endosymbiosis. This single- robust as vision, but the creatures using those celled organism with its new chloroplast was the fi Department of skills would argue otherwise. Why does vision rst cell to use this rather narrow band of the Ophthalmology & Vision sun’s emissions to produce energy. This process Science, University of exist at all? And why is it so dominant at least California, Davis, in the number of species that rely upon it for would eventually green the planet, and Sacramento, CA, USA their principal sensory mechanism? How did permitted the production of beta carotene— vision begin? What were the important steps in essential to the production of retinal for the Correspondence: the evolution of eyes? How did eyes rhodopsin that would follow. IR Schwab, Department of differentiate along their various paths, and why? Ophthalmology & Vision – Science, University of Eye (2018) 32, 302 313; doi:10.1038/eye.2017.226; Opsins The opsin in rhodopsin probably California, Davis, 4860 Y published online 20 October 2017 evolved from a G-protein coupled receptor Street, Suite 2400, (GPCR) protein although this origin is murky.3 Sacramento, CA 95817, USA G proteins are rather common and rather easily Tel: +916 734 6071; produced, but the first ‘opsins’ were not true Fax: +916 734 0411. GPCR. Rather these early opsin-like compounds E-mail: irschwab@ The ocular toolkit combined with retinal that functioned as a ucdavis.edu proton pump for energy production for certain Selection of visually responsive compounds Archaea.4,5 The passage of such molecules from Received: 27 July 2017 fi Accepted: 31 July 2017 Retinal Life probably rst appeared ~ 3.7 microbial opsins to metazoan opsins probably Published online: billion years ago as a simple cell with the ability came from a common ancestor as these are 20 October 2017 to replicate. Current extant cyanobacteria related, albeit distantly.5 The evolution of eyes IR Schwab 303 — Figure 1 Stromatolites are alive today and this small formation Figure 2 Nereis virens King sandworm: note the eyecup but no from Shark Bay in Western Australia illustrates the oxygen that is lens. This provides some spatial information for the animal given off by the cyanobacteria that compose the stromatolite. although its vision is poor. Nevertheless, it is a predator. Histologic section by Richard Dubielzig DVM. Formation of an eye Retinal and its eventual congeners and an opsin served as the basis for the principal family of metazoan From an eyespot to a simple eye photoreceptive compounds—the ciliary opsins, Once an opsin (or the predecessor of the opsins) 6 rhabdomeric opsins, and the photoisomerases. These covalently bonded with retinal, perhaps in a cell with a were not the only photoreceptive compounds available to cilium or two, the slow crawl to an eye began. Instead of fi fl rst life as other compounds such as the avins, studding the cellular membrane with bacteriorhodopsin porphyrins, biliproteins, and chlorophyll among others as might be seen in Halobacterium solarium, these fi could have been suf cient for the transduction of light to compounds came together in an eyespot, and evolution the energy to power a biochemical signal. However, co-opted the molecule for sight instead of using it as a under certain circumstances these compounds could be proton pump. toxic or photosensitizing to cells. These other compounds Multiple light-sensing cells in an eyespot in a were not able to compete as successfully with rhodopsin multicellular animal, such as a leech could recognize only for the principal photoreceptive one although the light or dark. Perhaps after 35 000 generations, an flavins are retained in many Metazoa as light-sensing organism discovered that developing a concave cup molecules in the form of cryptochromes.7,8 This instead of a spot produced a more successful and 12 biochemistry was crucial to our use of rhodopsin and competitive organ for sight. 12 cryptochromes. As Nilsson and Pelger suggested, from an eyespot to an eyecup to a fully formed camera-style eye could take as few as 364 000 generations, and the production of such Genetic anlage Certainly, rhodopsin is essential to the an eye in perhaps as short a period as half a million years. eventual evolution of eyes, but that is only a start. The Pax Of course, there would be more to an eye than just a cup, gene family joined the party although in a primitive form but that is a key step (Figure 2), and that cup may fit the and gradually evolved. The predecessor of these ancient real definition of an ‘eye.’ If one assumes that the eye genes can be found in organisms as basal as some must provide spatial information to be defined as an eye, sponges9,10 and some cnidarians (the jellies) as PaxB. then the curvature of a cup would create the first eye, as Jellies (better named as jellies as these are not fish) are not primitive spatial information would be provided. Such an considered in our lineage meaning that the last common eye can be seen in the limpet.13 Progress toward a more ancestor of jellies and most other metazoan creatures typical eye could proceed quickly in geological terms with must have had a similar protein that was eventually the sides of the cup creating a pinhole as can be seen in bequeathed to all triploblasts11,12 because we did not the abalone13 or the nautilus eye14 (Figure 3). Crystalline descend from the jellies. lenses were added later on in the eye’s evolutionary With the combination of retinal as a chromophore, and history. This explains why different lineages have an opsin with a GPCR structure, and with the genetic surprisingly different compounds composing their lenses. anlage to make an eye, the toolkit had begun. Trilobites have calcite, invertebrates have recruited a Eye The evolution of eyes IR Schwab 304 Figure 3 Nautilus: note the nautilus eye with a pinhole but no Figure 4 Dragonfly sp. Note the multiple ommatidia. Many cornea. The eye is embedded with the body with the histology species have ~ 30 000 individual hexagonal units with a seen in Figure 8. horizontal band of smaller and more concentrated ommatidia for a finer image. variety of crystallins and some novel proteins,15 and vertebrates have a wide variety of somewhat similar individual unit of a compound eye, called an crystallins, mostly heat-shock proteins.16,17 Evolution has ommatidium (pl. ommatidia Gr. ‘little eyes.’) Multiple selected whatever enzyme or heat-shock protein was such ommatidia would likely have been produced by available, often co-opted from other functions, to design gene duplication eventually leading to as many as 30 000 and fashion metazoan lenses. This indicates that lenses individual units as found in a dragonfly (Figure 4). are relative latecomers in the development of the eye, and The morphology of the compound eye would itself are often taxon-specific. As these compounds are evolve and radiate into at least six general categories biochemically different, they differ in their ability to be (some of the general categories have subcategories) of deformed. Fish lenses, for example, are quite hard and compound eyes, including these: (1) apposition; (2) afocal deform very little, but most avian lenses are soft and quite apposition; (3) neural superposition; (4) refracting ductile. superposition; (5) parabolic superposition; and (6) reflecting superposition.19 From an eyespot to a camera-style eye Each of these models provides different optics and neurologic channels necessary to fit the niche represented.