Sea urchins use their entire body as an eye

Purple sea urchins look like beautiful pincushions. They have no obvious eyes among their purple spines, but they can still respond to light. If you shine a spotlight on one, it will sidle off to somewhere darker. Clearly, the purple sea urchin can see, and over the past few years, scientists have worked out how: its entire body is an eye.

For decades, scientists knew that sea urchins can respond to light, even though they don’t have anything that looks remotely like an eye. The mystery deepened in 2006, when the full genome of the purple sea urchin was published. To everyone’s surprise, its 23,000 genes included several that are associated with eyes. The urchin has its own version of the master gene Pax6, which governs the development of animal eyes from humans to flies. It also has six genes for light-sensitive proteins called opsins.

While these genes are usually switched on in the developing eye, Maria Arnone found that the sea urchin’s versions are strongly activated in its feet. Sea urchins have hundreds of “tube feet”, small cylinders that sway around amid the spines. They can use the feet to move around, to manipulate food, and apparently to see.

Esther Ullrich-Luter – one of Arnone’s collaborators – found that each foot has two clusters of light-sensitive cells: one at the tip and another at its base. Each foot has up to 140 of these cells, giving a total of 200,000 across the entire animal. (For comparison, humans have a thousand times as many.)

The light-sensitive cells connect to a single nerve running down the length of each foot. The nerves of the tube feet eventually cluster into five spokes, which meet at a central ring of nerves. This is the extent of the urchin’s nervous system – it’s a sparse network of nerves without any central brain. Through this network, the sea urchin detects can react to light, which it spots with its hundreds of feet.  Its entire surface is effectively a big compound eye.

These discoveries revealed how the urchin sees, but they raised a new mystery. The urchin can clearly tell where a source of light is coming from, because it can move in the opposite direction. But the tube feet move about a lot, so they ought to pick up light from almost all directions. How can the urchin sense the direction of light?

Sönke Johnsen suggested that answer lies in the urchin’s spines , which shade specific parts of its body. That might be true, but Ullrich-Luter has found that another body part provides the necessary shade – the skeleton. Sea urchins have a hard internal shell within their body. The nerves of the tube feet pass through pores in this shell, and next to these pores, there are small dents. Some of the urchin’s light-sensitive cells lie within these dents (the red patches in the image below). These clusters are shaded from most directions – only a few cells are hit by light at any one time. By using the shadow of its own skeleton, the sea urchin can work out where a source of light is coming from.

Ullrich-Luter confirmed her idea by showing that baby sea urchins, which haven’t grown a skeleton, don’t shy away from light. Their skeletons only develop a month into their life, and their tendency to steer clear of light turns up at the same time.

If the idea of hundreds of foot-eyes that see using skeletal shadows wasn’t weird enough, the sea urchin’s odd eyes hold one last mystery – they seem to be built from the wrong parts. There are two major branches of the animal family tree and, until recently, it seemed that each branch built their eyes using one of two light-sensitive cells. The “protostomes” including insects and other arthropods have “rhabdomeric” light sensors, while the “deuterostomes”, including us and other back-boned animals, have “ciliary” sensors.

The sea urchin has the rhabdomeric type, which is very strange because it’s a deuterostome – it’s more closely related to us than to any fly or spider. There are a few examples of rhabdomeric cells in vertebrates, but they’re not used for vision – they’re mostly used to control body clocks. The purple sea urchin is the exception. It suggests that rhabdomeric light-detectors have been the norm for eyes, throughout much of the animal kingdom’s history. Only in the vertebrates have these cells abandoned their old roles, which were taken up by the ciliary cells.

Reference: Ullrich-Lüter, Dupont, Arboleda, Hausen & Arnone. 2011. Unique system of photoreceptors in sea urchin tube feet. PNAS http://dx.doi.org/10.1073/pnas.1018495108

Photos: by Maria Arnone andMinette Layne