Ian Musgrave has just posted an excellent article on the poor design of the vertebrate eye compared to the cephalopod eye; it’s very thorough, and explains how the clumsy organization of the eye clearly indicates that it is the product of an evolutionary process rather than of any kind of intelligent design. A while back, Russ Fernald of Stanford University published a fine review of eye evolution that summarizes another part of the evolution argument: it’s not just that the eye has awkward ‘design’ features that are best explained by contingent and developmental processes, but that the diversity of eyes found in the animal kingdom share deep elements that link them together as the product of common descent. If all we had to go on was suboptimal design, one could argue for an Incompetent Designer who slapped together various eyes in different ways as an exercise in whimsy (strangely enough, though, this is not the kind of designer IDists want to propose)…but the diversity we do see reveals a notable historical pattern of constraint.

How different are animal eyes? In the metazoans, about a third of all phyla don’t have any eyes at all, although light sensitive molecules are ubiquitous (for example, in sea urchin tube feet), and can be found in bacteria and, obviously, plants.

Another third of the metazoan phyla have light sensitive organs, specialized epithelial patches that respond to changes in light levels. They may have some morphological specializations, but they don’t focus an image in any way, and can’t resolve patterns of light.

The rest have distinct, image-forming eyes that focus light on an array of light-sensitive cells, and can detect patterns of light and shadow that are used to perceive a picture of the world around them. For us motile animals, eyes seem to be part of the recipe for success—the six animal phyla (cnidaria, mollusca, annelida, onychophora, arthropoda, and chordata) that contain 96% of all animal species also primitively evolved eyes.

These animal eyes fall into two major categories, with further subdivisions. Chambered eyes have a single optical element—a slit, a lens, a mirror—and focus an image on a 2-dimensional array of photoreceptors, the retina. Compound eyes use multiple optical elements.

Eight major types of optics in animal eyes. Both chambered eyes (top) and compound eyes (bottom) form images using shadows (A and B), refraction (C to F), or reflection (G and H). Light rays shown in blue, photoreceptive structures are shaded. The simple pit eye (A) (chambered nautilus) led to the lensed eyes in fish and cephalopods (C) (octopus) and terrestrial animals (D) (red-tailed hawk). Scallop eyes (G) (bay scallop) are chambered but use concave mirror optics to produce an image. The simplest compound eye (B) (sea fan) found in bivalve molluscs led to the apposition compound eye (E) (dragonfly) found in bees, crabs, and fruit flies; the refracting superposition compound eye (F) (Antarctic krill) of moths and krill; and the reflecting superposition eye (H) (lobster) found in decapod shrimps and lobsters. [Sources: (A) Wikipedia; (B) Robert Pickett/CORBIS; (C) Russell Fernald/Stanford University; (D) Steve Jurvetson/Wikipedia; (E) David L. Green/Wikipedia; (F) Gerd Alberti, Uwe Kils/Wikipedia; (G) Bill Capman/Augsburg College; (H) Lawson Wood/CORBIS]

Eyes can be further categorized as rhabdomeric or ciliary by the nature of the cellular elements that make up the photoreceptors, by the kind of opsin molecule used to transduce the light signal, and by the signaling pathway used to convert a conformation change of the opsin molecule into a change in the electrical potential across the cell membrane.

Schematic illustration showing the key differences between simplified representations of (top) canonical vertebrate ciliary phototransduction and (bottom) invertebrate rhabdomeric phototransduction, where hn represents incident photon energy. The two different opsin types (c-opsin and r-opsin) are contained in distinctly different membrane types, ciliary and rhabdomeric. The opsins are coupled to different families of G proteins that act via different types of transduction cascades. Amplification occurs during phototransduction in ciliary receptors and during channel opening in rhabdomeric receptors. These cascades produce signals of different sign. Gt, transducin; PDE, phosphodiesterase; cGMP, cyclic guanosine monophosphate; Gq, guanine nucleotide-binding protein α15; PIP2, phosphatidylinositol 4,5-bisphosphate; DAG, diacylglycerol.

Whoa…the differences are all over the place. Eyes look different, function differently, develop differently, and use different molecules, so where are the signs of common descent? The differences tell us that eyes have arisen in evolutionary history multiple times, but there are still deep homologies; in particular, look at those opsins, specifically the Type 2 opsins.

A simplified schematic molecular phylogenetic tree inferred by the neighbor-joining method showing the seven known opsin subfamilies. Three families transduce light using G protein-coupled mechanisms (Gq, Gt, Go); the best known are Gq or r-opsins found in invertebrate photoreceptors and Gt or c-opsins found in vertebrate photoreceptors. Encephalopsin and its teleost homolog tmt are found in multiple tissues with unknown function. Pinopsins, closely related to c-opsins, are expressed in the pineal organ of several vertebrates, and vertebrate ancient opsins are expressed in nonphotoreceptor retinal cells, including amacrine and horizontal neurons in teleost fish retinas. Similarly, neuropsins are found in eye, brain, testes, and spinal cord in mouse and human, but little is known about them. Peropsins and the photoisomerase family of opsins bind all-trans-retinal, and light isomerizes it to the 11-cis form, which suggests a role in photopigment renewal. These are expressed in tissues adjacent to photoreceptors, consistent with this role. Recent data suggest that some cold- blooded vertebrates have an additional opsin type, named parietopsin because it is found only in parietal eye photo-receptors.

It’s one big happy gene family, with members all related to one another. The major family members are the r-opsins, used in the rhabdomeric eyes of invertebrates, and the c-opsins, used in the ciliary eyes of vertebrates, but note that there is considerable overlap. We vertebrates also have an r-opsin: melanopsin is a visual pigment molecule expressed in ganglion cells (not classically considered photoreceptors) in our eyes, and are involved in detecting general light levels to reset our circadian clocks. Some invertebrates have both rhabdomeric and ciliary eyes and use both r-opsin and c-opsin in vision. Note also that some of these opsins have unknown functions—neuropsin, for instance, is expressed in human testes, a curious pattern that makes me wonder if there’s some analogy that could be made with the tube feet of sea urchins.

You might argue that the relationships are all spurious—maybe there is only one chemistry possible for transducing photons into a chemical signal (which is absurd on the face of it, but let’s be thorough and make the suggestion anyway). That’s easily countered: those are Type 2 opsins, what about Type 1? Type 1 opsins are found in the Archaea and in eukaryotic microbes, and while both Type 1 and Type 2 interact with retinal, Type 1 opsins have a different molecular size, a different structure, and a different function—they couple photoreception to transmembrane ion pumping, rather than to activation of a G protein signal transduction cascade. The similarities of these various phototransduction molecules are not necessary outcomes of their function, but instead reflect a contingent historical connection between them. We can put together a good explanation for these relationships with evolutionary theory.

Taken together, these data show that at least two kinds of photoreception existed in the Urbilateria, before the split into three Bilateria branches at the Cambrian. Moreover, each branch of the family tree still carries versions of both of these photoreceptor types, along with other opsin-dependent photodetection systems yet to be fully described. In the course of evolution, vertebrate vision favored ciliary photodetection for the pathway that delivers images, whereas invertebrates favored rhabdomeric photodetection for their main eyes, although why this might be remains unknown. Along both evolutionary paths, secondary photodetection systems remained to give additional information about light, possibly to instruct circadian rhythms, phototaxis, or other light-dependent behaviors. But, if vertebrates are an example, these two photodetection systems functioned together, rather than remaining separate. Although the remaining five families of opsins have not been fully characterized, it seems probable that they also respond to light, and organisms use the information they provide.

One other thing that I would note from these examples is illustrated by the c-opsin and r-opsin pathways. These are “molecular machines” or “biochemical pathways” of the sort that Intelligent Design creationists like Behe talk about, but they don’t dig into the specifics of these because they undercut their point. I look at pathways like the c-opsin → phosphodiesterase (PDE) vs. r-opsin → phosphatidylinositol (PIP) pathway, and what I see are two common signal transduction pathways (PDE and PIP show up in lots of other places, too) that have been coupled to slightly different sensors. What we find in molecular biology is flexibility and modularity, attributes that lend themselves well to combinatorial changes that can easily increase complexity—a complexity that is a hallmark of unguided evolutionary change, not design.

Fernald RD (2006) Casting a genetic light on the evolution of eyes. Science 313:1914-1918.


  1. #1 Owlmirror
    February 23, 2008

    The original publication has been made freely downloadable from the author’s website:

    He has lots more interesting publications, mostly on fish:

    There’s an amusing quote on his lab webpage:

    “If you wish to be a success at Stanford, work on fish. Jordan himself, when he works at all, works on fish… The physiologist… works on fish… The geologists, the paleontologists, the botanists, the English department, the Romance languages, even the philosophers – they all work on fish. Go there my boy, be happy, and work on fish.”

    [-Professor Loeb speaking to Hans Sinsser about success at Stanford, ca. 1892]

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