Masters of disguise, many cephalopods think nothing of changing their skin colour to blend in with the surroundings. ‘These changes primarily rely on eyesight’, say Desmond Ramirez and Todd Oakley from the University of California, Santa Barbara, USA, who explain that octopuses collect information about their setting with their large camera-like eyes before sending signals to chromatophores in the skin to change colour. However, Ramirez had noticed two reports describing how the colour-changing structures (chromatophores) in tiny biopsies of squid and octopus skin reacted to light with no input from the eyes or brain; although no one had followed up on the observations. Meanwhile, Alexandra Kingston and Thomas Cronin from the University of Maryland, Baltimore County, USA, were also pondering the possibility that cephalopod skin may respond to light because other biological structures are known to detect light. In addition, they also knew that proteins – so-called non-visual opsins that are analogous to the opsin proteins that sense light in eyes – are produced in the skin of various animals. Intrigued by the possibility that cephalopod skin is sensitive to light, both teams embarked on independent studies to see if they could identify key components of the light-sensing mechanism found in eyes in the skins of octopus, squid and cuttlefish.
Collecting skin biopsies from California two-spot octopuses, Ramirez and Oakley first shone white light on the tissue and were impressed to see the colour-changing chromatophores expand when light fell on them and relax when the light went off, returning the skin to its original hue. Then, they measured how long it took the chromatophores to expand to change the skin's colour when exposed to light ranging in colour from violet to orange, finding the swiftest response to 480 nm light (blue), which coincides with the wavelength of light that the octopus's eye opsin responds to most strongly. Referring to the light reponse as light-activated chromatophore expansion (LACE), the duo then tested the skin for evidence of expression of opsin genes, and they were pleased to find expression of the gene for rhodopsin, the opsin protein that is usually produced in the eye. And when the duo tested where the rhodopsin protein was produced in the skin, they found it localised to sensory neurons distributed on the mantle surface.
Focusing on several cephalopods – two cuttlefish and a squid – Kingston and Cronin decided to investigate whether they could identify components of the molecular machinery that is essential for converting light detection into a behaviour. As they knew that light activates rhodopsin in the retina, triggering a cascade of protein interactions that culminate in an ion channel opening to signal light detection, the pair of scientists began searching for key proteins in the rhodopsin signalling cascade in the skin of the common cuttlefish, the broadclub cuttlefish and the longfin inshore squid. Using a battery of molecular techniques, Kingston and Cronin identified rhodopsin in the skins of both cuttlefish and the squid, and they also found other proteins that are essential for the light sensing in the animals’ skin. Next, they teamed up with Alan Kuzirian and Roger Hanlon to look in closer detail at chromatophores isolated from different regions of the squid's mantle and found that the light-sensing cascade proteins were actually in the chromatophores. ‘The very same structures that show behavioral responses are actually themselves light-sensitive’, says Cronin.
So, both teams present compelling evidence that cephalopods may have adapted the cellular mechanism that detects light in eyes for light sensing in skin, and Ramirez and Oakley have collected the first recording of the skin's sensitivity across the visual spectrum. In addition, Kingston and Cronin suggest that squid chromatophores directly sense the light that they respond to through three possible mechanistic scenarios: they could interact directly with adjacent cells, through the gap junctions between muscle cells or through nerve fibres to communicate with the central nervous system, providing information about the animals’ surroundings while it tries to blend in.