How many genes does it take to make a squid eye?

This is an article about cephalopods and eye evolution, but I have to confess at the beginning that the paper it describes isn't all that interesting. I don't want you to have excessive expectations! I wanted to say a few words about it, though, because it addresses a basic question I get all the time, and while I was at it, I thought I'd mention a few results that set the stage for future studies.

I'm often asked to resolve some confusion: the scientific literature claims that eyes evolved multiple times, but I keep saying that eyes show evidence of common origin. Who is right? Why are you lying to me, Myers? And the answer is that we're both right.

Eyes evolved independently multiple times: the cephalopod eye evolved about 480 million years ago, and the vertebrate eye is even older (490 to 600 million years), but both evolved long after the last common ancestor of molluscs and chordates, which lived about 750 million years ago. The LCA probably did not have an image-forming eye at all.

And that's the key point: a true eye is a structure that has an image forming element, a retina, and some kind of morphological organization that allows a distant object to form a pattern of light on that retina. That organization can be something as simple as a cup-shaped depression or pinhole lens, or as elaborate as our camera eye, or an insect's compound eye, or the mirror eyes of a scallop. An eye is photoreceptors + structure. Eyes have evolved multiple times; they've even evolved multiple times within the phylum Mollusca, and different lineages have adopted different strategies for forming images.

i-0f6286e48f36b86c30ae81bdbfc6f415-eye_phylo-thumb-500x210-70144.jpeg
(Click for larger image)

Phylogenetic view of molluscan eye diversification. Camera eyes were independently acquired in the coleoid cephalopod (squids and octopuses) and vertebrate lineages.

The LCA probably didn't have an eye, but it did have photoreceptors, and the light sensitive cells were localized to patches on the side of the head. It even had two different classes of photoreceptors, ciliary and rhabdomeric. That's how I can say that eyes demonstrate a pattern of common descent: animals share the same building block for an eye, these photoreceptor cells, but different lineages have assembled those building blocks into different kinds of eyes.

Photoreceptors are fundamental and relatively easy to understand; we've worked out the full pathways in photoreceptors that take an incoming photon of light and convert it into a change in the cell's membrane properties, producing an electrical signal. Making an eye, though, is a whole different matter, involving many kinds of cells organized in very specific ways. The big question is how you evolve an eye from a photoreceptor patch, and that's going to involve a whole lot of genes. How many?

This is where I turn to the paper by Yoshida and Ogura, which I've accused of being a bit boring. It's an exercise in accounting, trying to identify the number and isolate genes that are associated with building a camera eye in cephalopods. The approach is to take advantage of molluscan phylogeny.

As shown in the diagram above, molluscs are diverse: it's just the coleoid cephalopods, squid and octopus, that have evolved a camera eye, while other molluscs have mirror, pinhole, or compound eyes. So one immediate way to narrow the range of relevant genes is a homology search: what genes are found in molluscs with camera eyes that are not present in molluscs without such eyes. That narrows the field, stripping out housekeeping genes and generic genes involved in basic cellular processes, even photoreception. Unfortunately, it doesn't narrow the field very much: they identified 5,707 candidate genes that might be evolved in camera eye evolution.

To filter it further, the authors then looked at just those genes among the 5,707 that were expressed in embryos. Eye formation is a developmental process, after all, so the interesting genes will be expressed in embryos, not adults (a sentiment with which I always concur). Unfortunately, development is a damnably complicated and interesting process, so this doesn't narrow the field much, either: we're down to 3,075 candidate genes.

Their final filter does have a dramatic effect, though. They looked at the ratio of non-synonymous to synonymous nucleotide changes in the candidate genes, a common technique for identifying genes that have been the target of selection, and found a grand total of 156 genes that showed a strong signal for selection. That's 156 total genes that are different between coleoids and other molluscs, are expressed in the embryonic eye, and that show signs of adaptive evolution. That's manageable and interesting.

They also looked for homologs between cephalopod camera eyes and vertebrate camera eyes, and found 1,571 of them; this analysis would have been more useful if it were also cross-checked against other non-camera-eye molluscs. As it is, that number just tells us some genes are shared, but they could have been genes involved in photoreceptor signalling (among others), which we already expect to be similar. I'd like to know if certain genes have been convergently adopted in both lineages to build a camera eye, and it's not possible to tell from this preliminary examination.

And that's where the paper more or less stops (I told you not to get your hopes up too high!) We have a small number of genes identified in cephalopods that are probably important in the evolution of their vision, but we have no idea what they do, precisely, yet. The authors have done some preliminary investigations of a few of the genes, and one important (and with hindsight, rather obvious) observation is that some of the genes are expressed not just in the retina, but in the brain and optic lobes. Building an eye involved not just constructing an image-forming sensor, but expanding central tissues involved in processing visual information.


Fernald RD (2006) Casting a genetic light on the evolution of eyes. Science 313(5795):1914-8.

Yoshida MA, Ogura A (2011) Genetic mechanisms involved in the evolution of the cephalopod camera eye revealed by transcriptomic and developmental studies.. BMC Evol Biol 11:180.

(Also on FtB)

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