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Logo of brjopthalBritish Journal of OphthalmologyVisit this articleSubmit a manuscriptReceive email alertsContact usBMJ
Br J Ophthalmol. 2007 September; 91(9): 1107–1108.
PMCID: PMC1954945

An out‐pouching of the eye?

The eye had to start somewhere. Of course, much depends on how one defines an eye. In the long course of evolution, sensory mechanisms began slowly, and many components probably were co‐opted from functions distinct from those eventually used for any particular sensatory mechanism.

To be defined as an eye, a structure must be stimulated by light with the recognition of gathered spatial information. The sense of olfaction is triggered by a molecular stimulus, and may lead to a response. To be a brain, a collection of neurons must receive information in the form of electric potentials, integrate the information and contribute to a motor output.

Photoreception, in its most rudimentary form, probably began very early in life's history. The sun provided at least one of the sources of the energy that permitted life to begin and flourish. Vitamin A, or retinal, is a molecule that was incorporated into the cell membrane of some single‐celled animals first populating the hellacious earth 3.8 billion years ago. Incorporation of retinal, a proton pump and simple energy source, conferred a distinct advantage over those cells that did not have such an energy source. Did such concentrations of retinal in membranes of single cells constitute the first eye? Similarly, noxious chemicals would destroy a nascent cell membrane, and avoidance would be essential for preservation. Would the recognition and avoidance of these many noxious chemicals have come from the first “nose?” Neither negative nor even positive trophic responses toward light would seem to qualify for “real” vision as spatial resolution is at the core of any true visual system. For such spatial capabilities, there would need to be an organised system of collection and storage of sensory information. Such collection and storage probably provided the basis for the beginning of a brain. Since the potential for spatial resolution is much greater for light and the speed of light is faster than that of odour plumes, the initial organisation of sensory information must have begun around vision.

Prokaryotic eubacteria thrived for eons. Archaea joined the eubacteria at some time either by evolution, or began again, perhaps at the oceanic vents. Archaea were dramatic prokaryotes that incorporated retinal into their membranes—at least at some point—as some of these still retain these transmembrane compounds. Presumably, then, some of the early components of the eye, but not necessarily an eye, were present from the dawn of life.

The development of a nucleus was key to metazoan life because it allowed for the organisation of the protein coding system. The nucleus was, after all, a repository of information—a cellular tutorial. This is a biochemical library and instruction system, but hardly a brain.

The eukaryotes (nucleated cells) progressed in diverse ways and left extant generational diaspora. One such line of unicellular evolution has led to the dinoflagellates and, in particular, Warnowia (Cover upper left). This animal, and its close relatives, has an eye, a structure no one would deny as a rudimentary eye, even though it is entirely subcellular.1 Yet, it has no brain. No one knows exactly how this creature transmits the signals it receives from its eye to its flagellum, but it must do so for it is a predator of other dinoflagellates. Clearly, no “brain” is necessary.

Single‐celled eukaryotes must have ruled the earth longer than any other group, apart from perhaps the prokaryotes. Nevertheless, these single‐celled organisms discovered that cooperation led to more robust organisms—and primitive sponges were born. Sponges probably begat jellyfish. Such multicellular aggregations may have become possible because of the eukaryote acquisition of mitochondria through the cellular symbiosis of prokaryotes. In attaining mitochondria, the eukaryote acquired much more than the efficient consumption of oxygen and production of ATP. These ex‐prokaryote mitochondria contained all manner of long‐evolved killing capabilities and so the combined system could now be tweaked to control proto‐apoptosis.2 As any sculptor knows, it is the removal of the medium that allows refined forms to be created, so with this acquisition of apoptosis, multicellular animals were possible. And with multicellularity, it became possible to create greater complexities in neural connections. These, in turn, allowed for the integration of sensory input across space and time.

Jellyfish, likely the first motile metazoa, evolved 700 million years ago and remain with us today. Some have eyes, but none has a brain by most definitions. These diploblasts (two cellular layers) have neural nets that could be perceived as a primitive brain, but there is no central control, and the output is completely reflexive in nature. There is little processing of the neuronal input, which is limited to spatial relaying. Some of these creatures have surprisingly sophisticated camera‐style eyes, with working pupils, lenses and a retina in a curved cup‐like structure—in other words an eye. A neuroscientist might call the jellyfish's neural net a brain, but only because it satisfies the most rudimentary of definitions, and the eye is far ahead of it (Cover image lower left is Tripedalia cystophora and lower right is one of its eyes).

Invertebrates continued in other directions through the sponges and jellyfish to the worms. Primitive worms may have been similar to jellyfish with simple reflex arcs reacting to sensory input. But, it is here, arguably, that the first brain appeared—somewhere in the annelids, perhaps sometime around the cusp of the Ediacaran period approximately 650 million years ago. The important element in the Ediacaran was the formation of the third layer—triploblasts. Worms cannot perambulate without muscles, which require another layer. Preserved meandering tracings in the Ediacaran sands mean that the creature that laid down these small tracks had muscles. Actin and myosin are ancient compounds too, so we cannot assume that this was the first appearance of these proteins, but this may have been the first time metazoans used these proteins for directed perambulation.

But, why acquire a third layer? This had to be relatively “expensive” on an evolutionary and metabolic level. What would induce a creature to co‐opt actin/myosin into an entirely new layer? Evolutionary success is always the answer. The better question is “where were these worms going and why?”

Over and over again the real message throughout natural selection is “nutrition and reproduction.” Animals evolve to compete for these two basic activities. Any advantage that improves the prospects for either one of these objectives will be overwhelmingly favoured. So, how does any organism realise that there is nutrition or a mate separate from itself? No evidence remains to answer that question directly, but there surely were some variety of olfactory and/or visual sensory stimuli to lead one worm to another or to food. Once the sensory mechanism became organised, storage and decision making had to follow, especially if muscular elements would require an organised output. This still does not guarantee a brain, though.

The Ediacaran era led to the Cambrian era about 543 million years ago. The Cambrian explosion is the “big bang” of evolution possibly because of increased oxygen levels. Whatever the reason, though, there was an explosion of phyla, the likes of which the earth had never seen before or since. One of the phyla that evolved was Arthropoda and included the molluscs. Molluscs include bivalves such as clams and scallops. Interestingly, the same scallops enjoyed in “haute cusine” have multiple eyes with lenses, a two‐tiered retina and sophisticated mirror optics—but no brain (Cover image upper right). Rather, these edible delicacies have a neural net that interacts with the muscular foot enjoyed by so many. This would suggest that whatever common ancestor preceded the arthropod diversity probably did not have a brain or, less likely, that the brain has been lost for scallops. Certain clams have three types of photoreceptors and perhaps some form of, or at least the capability of, colour discrimination, but no brain to compare these signals. It is not likely that these giant clams would have different receptors without using them for colour vision. Even the sophisticated process of the comparison of signals necessary for colour discrimination does not seem to proceed in these giant clams. This means that although a true brain may have evolved in the annelids during the Ediacaran, there are other phyla that proceeded into the Cambrian and beyond, even to modern times with sophisticated eyes but no real brain to take full advantage of these eyes. Of course, molluscs continued to evolve in other directions with surprisingly intricate eyes. The octopus, for example, has a camera style eye with a spherical lens, iris diaphragm and retinal architecture,3 as well as an excellent brain.

Vertebrates may have started with protochordates from the Cambrian with predecessor annelids from the Ediacaran,4 and this may have been a key pivotal organism for vertebrates. These protochordates probably included a brain by current definitions, and this may have contributed to vertebrate success.

Sensory mechanisms, with the eye as a prominent proxy, led to and probably preceded the brain, at least as currently defined. There is no reason to have a repository for information without the input of complex and rapidly changing information that requires storage.

Homeobox genes that control the eye also provide control for brain elements. As is often the case, evolution re‐invents new applications for homologous systems. Not surprisingly, certain brain structures, such as the cerebellum, repeat retinal organisation, such as the Purkinje cell, which resembles the retinal ganglion cell in anatomy and biochemical features.

So, what does all this mean? Sensory input, with vision as the most prominent proxy, probably pushed the evolution of the brain.

Andrew Parker, in his book In the Blink of an Eye,5 also believes that vision drove evolution. It cannot be that simple, of course, as there must have been many forces from climate, meteor strikes, new forms of competition and the serendipity of simple chance. Nevertheless, sensory input must have been critical in driving evolution. Sensory input, particularly vision, probably improved in sophistication in tandem or co‐evolution with neurological change since the sensory input could not be useful to the organism without the necessary machinery to understand and translate that input. Conversely, there would be no need for such neurological machinery if the sensory input were more pedestrian. Hence, photoreception led to the eye and this stimulated the formation of the necessary neurological equipment to decode, translate, organise, remember and integrate this sensory input.

And you probably thought the eye was an out‐pouching of the brain.


Competing interests: None.


1. Schwab I R. You are what you eat. Br J Ophthalmol 2004. 881113
2. Sadun A, Carelli V. The role of mitochondria in health, ageing, and diseases affecting vision. Br J Ophthalmol 2006. 90809–810.810 [PMC free article] [PubMed]
3. Schwab I R. A well armed predator. Br J Ophthamol 2003. 87812
4. Schwab I R. Can you keep a secret? Br J Ophthalmol 2005. 89795
5. Parker A. In the Blink of an Eye. Cambridge, MA: Perseus Publishing, 2003

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