Octopuses are well known for changing the colour, patterning, and texture of their skin to blend into their surroundings and send signals to each other, an ability that makes them both the envy of, and inspiration for, army engineers trying to develop cloaking devices. As if that wasn’t already impressive enough, research published today in the Journal of Experimental Biology shows that octopus skin contains the pigment proteins found in eyes, making it responsive to light.

These clever cephalopods can change colour thanks to specialised cells called chromatophores, which are packed in their thousands just beneath the skin surface. Each of these cells contains an elastic sac of pigmented granules surrounded by a ring of muscle, which relax or contract when commanded by nerves extending directly from the brain, making the colour inside more or less visible.

Octopuses are thought to rely mainly on vision to bring about these colour changes. Despite apparently being colour blind, they use their eyes to detect the colour of their surroundings, then relax or contract their chromatophores appropriately, which assume one of three basic pattern templates to camouflage them, all within a fraction of a second. Experiments performed in the 1960s showed that chromatophores respond to light, suggesting that they can be controlled without input from the brain, but nobody had followed this up until now.

Evolutionary biologists Desmond Ramirez and Todd Oakley of the University of California, Santa Barbara therefore removed patches of skin from 11 hatchling and adult bimac octopuses (Octopus bimaculoides), mounted them onto Petri dishes with insect pins, and used light emitting diodes to shine light of different wavelengths onto the skin preparations. They noticed that the chromatophores expanded quickly, and remained expanded, pulsating rhythmically, when exposed to continuous bright white light. By contrast, red light caused slow, rhythmic muscle contractions, but not chromatophore expansion.

In these, experiments, the chromatophores were most responsive to wavelengths of 480 nanometers (nm, or billionths of a meter), which corresponds to blue light. This also happens to be the wavelength that some opsins, the pigmented light-sensitive proteins found in eyes, absorb best. Ramirez and Oakley therefore predicted that opsins are present in octopus skin, where they might act as light sensors.

To test this, they stained some skin preparations with fluorescently-labelled antibodies that recognise and bind to opsins and other proteins that interact with them. Sure enough, they found that sensory neurons in the skin synthesize one version of the opsin protein, along with G protein alpha and phospholipase C, two enzymes that relay signals from opsin molecules that have been activated by light to the interior of the cell, and which are needed to initiate the cellular response.

Octopuses aren’t unique in this respect, as various other species are now known to have skin that contains opsins and is sensitive to light. But this study provides the first clear evidence that octopus skin is also sensitive to light, and also hints at a plausible mechanism by which chromatophores detect and respond to it.

Other research shows that the marine ragworm, a “living fossil” with primitive eyes consisting of patches of opsin-containing cells at the front of its brain, also expresses the same opsin protein in neurons located on the underside of its nerve cord, and in the hair-like appendages it uses to crawl and swim. These primitive creatures continue to avoid light after being decapitated, suggesting that the opsins found outside their brain are indeed involved in sensing light.

Ramirez and Oakley believe that octopus skin acts in a similar way. In eyes, opsins are arranged in an organized manner inside photoreceptor cells, so that they can recreate a faithful copy the visual field on the retina. In chromatophores, they are arranged loosely, and so light-sensitive skin would probably detect changes in brightness, rather than forming a detailed image.

The researchers also noted that the chromatophores in their skin preparations expanded in response to light touch as well as to light, and their antibody staining experiments revealed that they are expressed in the neurons that are sensitive to mechanical pressure. This raises the intriguing possibility that opsins, which have always been associated with vision, might also contribute to other senses. This is supported by recent studies showing that opsin is present in the fruit fly antenna, where it detects mechanical vibrations, and is critical for hearing.

It’s still not entirely clear whether octopus chromatophores act as light sensors, mechanical receptors, or both, but Ramirez and Oakley are planning to find out, in a series of new experiments designed to determine what kind of behaviours they are involved in. The fact that opsins are present in mechanically sensitive cells suggests they have a common and ancient role in these processes.

Ramirez and Oakley also plan to compare opsins from the skin and eyes of different species, in order to see how they are related, and to determine whether these non-visual light responses co-opted existing opsins, or evolved independently.

Reference

Ramirez, M. D. & Oakley, T. H. (2015). Eye-independent, light-activated chromatophore expansion (LACE) and expression of phototransduction genes in the skin of Octopus bimaculoides. J. Exp. Biol. doi: 10.1242/jeb.110908.