Octopuses, and Maybe Squid, Can Sense Light With Their Skin

Octopuses, squid, and cuttlefish, the animals collectively known as cephalopods, are capable of the most incredible feats of camouflage. At a whim, they can change the colour, pattern, and texture of their skins to blend into the background, baffle their prey, or communicate with each other.

As if that wasn’t amazing enough, Lydia Mäthger and Roger Hanlon recently discovered that the common cuttlefish has light-sensitive proteins called opsins all over its skin. Opsins are the engines of sight. Even though animal eyes come in a wondrous variety of shapes and structures, all of them use opsins of one kind or another. The discovery of these proteins in cuttlefish skin suggested that these creatures might be able to sense light over their entire surface, giving them a kind of distributed “sight”.

It was a tantalising suggestion, but far from a definitive one. Opsins are used in many other contexts, such as sensing the time of day, which still involve detecting light but have nothing to do with seeing images. To work out what exactly opsins are doing in cephalopod skin, the team needed more evidence.

For example, when opsins are struck by light, they change shape. This triggers a Rube Goldberg-esque chain of further changes in other proteins, which culminates in an electrical signal travelling through a nerve towards the brain. That’s the essence of vision. It’s what happens in a cephalopod’s eye. Does it also happen in their skin?

That’s exactly what Alexandra Kingston from the University of Maryland, Baltimore County decided to find out. Working with Hanlon and vision expert Tom Cronin, Kingston studied the skins of the longfin inshore squid, the common cuttlefish, and the broadclub cuttlefish, looking for proteins that act downstream of opsin.

She found them. Several of them are present in the animals’ skin, and only in the chromatophores—the cells that are primarily responsible for their shifting patterns. Each chromatophore is an elastic sac of pigment, surrounded by a starburst of muscles. If the muscles relax, the sac contracts into a small dot that’s hard to see. When the muscles contract, they yank the sac into a wide disc, revealing the colour it contains. Kingston showed that these living pixels contain the same Rube Goldberg set-up that exists in their owners’ eyes.

Her team couldn’t, however, show that the chromatophores actually respond to light. “All the machinery is there for them to be light-sensitive but we can’t prove that. It’s been very frustrating,” says Cronin. The chromatophores might be detecting local light levels to prime them for either expansion or contraction. They could communicate with each other so that small clumps of chromatophores react to light as a unit. Or they could send signals directly to the brain to provide their owners with more information about light levels in their environment. These possibilities could all be right or wrong; no one knows.

“We don’t know if they contribute to camouflage or are just general light sensors for circadian cycling or are driving hormonal changes. They have a job to do but we don’t know what it is,” says Cronin. “That’s biology!” he adds, resignedly.

Meanwhile, Desmond Ramirez and Todd Oakley from the University of California, Santa Barbara had better luck with a different cephalopod—the California two-spot octopus. When the duo shone bright light onto isolated patches of skin, they found that the chromatophores would dramatically expand. They called this light-activated chromatophore expansion, or LACE.

Ramirez and Oakley showed that the octopus’s skin also contains opsin, but not in the chromatophores. Instead, its opsins reside in small hair-like structures called cilia. People used to think that the octopus used these cilia as organs of touch; they still could be, but they might also detect light too. And echoing Cronin, Oakley says, “We don’t know yet how this is used, or indeed if it is used, in the living animal.”

Neither study is definitive, but they certainly complement each other. They strengthen the case that these animals really are detecting light with their skins, independently of their brains and eyes.

They also serve as useful reminders that cephalopods are a diverse group of very different animals, with different branches separated by over 280 million years of evolution. It shouldn’t be surprising that octopus skin readily responds to light, but squid and cuttlefish skin doesn’t seem to. Or that, in octopus skin, opsins are found in cilia, while in squid and cuttlefish, they live in chromatophores.

They behave differently, too. “Cuttlefish and squid do seem to display to each other more than octopuses,” says Cronin. “Octopuses do pattern dramatically in response to environmental changes, but we don’t know of displays in octopuses designed for other octopuses.” Perhaps each species uses its skin opsins for different tasks.

Reference: Ramirez & Oakley. 2015. Eye-independent, light-activated chromatophore expansion (LACE) and expression of phototransduction genes in the skin of Octopus bimaculoides. Journal of Experimental Biology http://dx.doi.org/10.1242/jeb.110908

Kingston, Kuzirian, Hanlon & Cronin. 2015. Visual phototransduction components in cephalopod

chromatophores suggest dermal photoreception. Journal of Experimental Biology. http://dx.doi.org/10.1242/jeb.117945