Sight without eyes

By Lauren Sumner-Rooney, Research Fellow

Vision is among the most important innovations in animal evolution. The ability to see predators, prey, mates, and the environment transformed the way animals interact with each other and the world around them. Eyes can take many different forms, but this month saw the description of a visual system unlike almost any other known to science, found in a brittle star called Ophiocoma wendtii.

Brittle stars are marine invertebrates related to starfish. They have long, slender arms connected to a central disk, but no head, no brain, and – so we thought – no eyes. But recent experiments have shown that some brittle stars are able to see the world around them.

Ophiocoma wendtii is a common species found throughout the Caribbean Sea and the Gulf of Mexico. If you rummage around in coral rubble in shallow water, you’ll probably find Ophiocoma hiding underneath rocks and other debris, sheltering from their fishy predators. It has beautiful bright red tube feet (small, water-filled tentacles) and a neat party trick: it changes colour. During the day, the animals are a deep reddish-brown colour, but after dark they become beige with dark stripes.

The red brittle star, Ophiocoma wendtii

For more than thirty years, O. wendtii has been something of a mystery to scientists like myself who are interested in animal vision. It’s covered in light-sensing cells – thousands of them – and it hates being exposed to bright light, quickly dashing for cover if possible. However, it’s possible to head for dark, shadowy places without vision; you only need to be able to tell that one direction is brighter than the other. So, with a team of colleagues from Germany, Sweden and the USA, we set about giving the brittle stars an eye-test.

Lauren Sumner-Rooney, collecting specimens of Ophiocoma wendtii. Image: Jane Weinstock

We know that when they’re exposed to sunlight, O. wendtii try to hide underneath nearby rocks or other objects, so we designed a circular arena with a stimulus printed on one side – the idea is that the stimulus might resemble an object under which the animals can shelter, and the animal will move towards it.

We ran three experiments, changing the stimulus and background of the arena in each to test whether the brittle star can just see relative light or dark areas, or whether it can resolve finer points of contrast. To my surprise, O. wendtii moved towards the stimuli in all three experiments significantly more frequently than expected by random chance, as you can see in the video below. This was super exciting, as it represents not only the very first evidence of vision in these animals, but the second known example of any animal that can ‘see’ without having eyes (the first is a close relative, a sea urchin).

While O. wendtii is known to shelter during the day, we were also curious to test its behaviour at night. Running the same experiments again in natural darkness, we found that animals no longer moved towards any of the stimuli. There could be a whole number of reasons behind this, so we devised tests that eliminated several possibilities, and were left with a remaining explanation that the animal’s colour-change between night and day was somehow responsible.

Close-up of the arm plates of Ophiocoma wendtii

Colour-changing in the brittle star is controlled by the expansion and contraction of cells, called chromatophores, that are filled with pigment granules. These sit inside pores in the skeleton, alongside the light-sensing cells. During the day, the chromatophores expand, pushing up through the pores and spreading over the body surface. The pigment is spread over the outside of the animal, which looks dark brown as a result. During the night, the chromatophores contract, bringing all the pigment granules back inside the skeleton and giving a paler appearance.

The red brittle star, Ophiocoma wendtii. Image: Heather Stewart

We thought that during the day the pigment granules surrounding the light-sensing cells might block light reaching them from most directions. To test this, we constructed digital models of the visual system, creating 3D models of the light-sensing cells, the skeleton, and the pigment granules.

We found that in light-adapted systems, those with pigment, light could only reach the sensory cells from an angle of around 60° out of 360° which, though probably very coarse, could support vision. By removing the pigment from the models, vision was made impossible, as light could reach the sensory cells from too many different directions. It looked as though it was the chromatophores that made all the difference.

This is the first proposed example of whole-body colour change enabling and disabling vision in any animal, and raises many new questions about image formation and information processing. There are exciting parallels with the only other example of ‘extraocular’ (=without eyes) vision, the sea urchin we mentioned earlier: these sea urchins can also change colour in response to light levels, using similar chromatophores. Have they independently evolved a similar trick?

Top image: Heather Stewart

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