Luminance control of neurally tuneable skin iridescence in squid

Abstract

Cephalopods create precise skin color and pattern displays for the purpose of signaling and camouflage. In squids, such visual trickery is achieved through the combined action of two color elements: pigmented chromatophores and structural iridophores (which produce iridescence). The neural control of chromatophores was recognized many decades ago but the system controlling dynamic iridescence remained in obscurity (although ACh was known to activate iridophores). To tackle this knowledge gap, we developed a novel physiological preparation in the squid Doryteuthis pealeii. Our results show that stimulation of dermal nerves shifts the spectral peak of the reflected light to shorter wavelengths (>145 nm) and increases the peak reflectance (>245 %) of innervated iridophores (Wardill et al. 2012). We also demonstrate that ACh is released within the iridophore layer and that extensive nerve branching is seen within each iridophore. The dynamic colour shift is significantly faster (17 s) than the peak reflectance increase (32 s) revealing two distinct control mechanisms. Responses from a structurally altered preparation indicate that the reflectin protein condensation mechanism (Izumi et al. 2010, Tao et al. 2010) explains the slower peak reflectance change, while a newly discovered water flux mechanism reducing platelet thickness (DeMartini et al. 2013) may explain the fast colour shift. Next, we traced the skin nerves towards the brain. While the chromatophore motorneurons descend directly from the brain, neural stimulation and dye back-filling revealed that cell bodies of the iridophore 'control' neurons are located in the stellate ganglion. Nonetheless, brain input is necessary for iridescence expression. Lastly, through behavioural tests, we showed that squids turn their iridescence on/off in response to lights on/off, respectively. However, the decline and rise of iridescence is slow, taking up to 1 hour and 5 minutes respectively, suggesting that iridescence may match light intensity during the diurnal cycle.