Hypothesis and homework

The paper traces the development of the vertebrate eye, from the bilateral ancestor of 580 million years ago, in which a primordial opsin - a visual protein that functions as a G-protein-coupled receptor - has evolved into three major classes: rhabdomeric opsins, intermediate photoisomerase-like opsins, and ciliary opsins. Here, protostomes with their rhabdomeric opsins separate from deuterostomes and our ciliary opsins.

Stage two is the development of the protochordates, about 580-550 million years ago, in which the ciliary photoreceptor with a ciliary opsin and a hyperpolarising response continue to evolve. Here, the cephalochordates and the tunicates - represented today by the lancelets and the sea squirt respectively - diverge.

Stage three is the ancestral craniates of 550-530 million years ago, in which a ciliary photoreceptor sends signals to output neurons, a primordial lens develops and the lateral 'eye' invaginates. The researchers say this proto-eye remains present in extant hagfish, which separated from our line 530 million years ago.

Then comes stage four, a period of about 30 million years, in which lamprey-like ancestors evolve and photoreceptors with cone-like features appear, along with an explosion in visual ability. Genome duplications give rise to multiple copies of the phototransduction genes, which allow light to be converted into electrical signals; cell classes diverge into five cone-like receptors; cone bipolar cells and ganglion cells evolve; ganglion-cell axons project into the thalamus and the optic equipment evolves - the lens, the iris and the extra-ocular muscles.

About 500 million years ago the lampreys - containing this modern equipment but lacking intra-ocular muscles - diverge from our line.

Stage five is a long period of about 70 million years in which the jawless fish give rise to the jawed vertebrates and the optic boom continues - rod photoreceptors and rod bipolar cells evolve, along with an iris that can adjust to different light levels. At stage six, 430 million years ago, the last jawless fish separate from the gnathostomes, in which the cornea develops, the lens takes an elliptical shape and eyelids appear.

While some would dispute the divergence of the hagfish and the lampreys, the researchers find evidence in the developmental changes that occur in the larval form of lampreys. This is a period of about five years in which the larval form, or ammocoete, metamorphoses into the adult. The eye of the ammocoete is strikingly similar to that of the hagfish - "they are small, they are buried beneath skin and they possess a relatively undifferentiated retina", they write - but over five years "a slow process of neural differentiation occurs, in the following sequence: ganglion cells, amacrine and horizontal cells, photoreceptors and finally bipolar cells. This is broadly the same order in which the jawed-vertebrate retina differentiates".

To back up their hypothesis, Lamb, Collin and Pugh have set us some homework. They have set out a series of eight predictions they say will test their hypothesis, encouraging other researchers to delve further into the development of cones, rods and bipolar cells, and in particular to study the genes of cyclostomes, to trace definitively when hagfish diverged. They are currently writing a grant application to assist with completing the homework.