Luminance control of neurally tuneable skin iridescence in squid
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1
Marine Biological Laboratory, Program in Sensory Physiology and Behavior, United States
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2
University of Texas Medical School at Houston, Department of Integrative Biology and Pharmacology, United States
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.
In summary: (1) Squid iridescence is neurally activated. (2) The color and reflectance changes follow different dynamics. (3) Iridophores and chromatophores are innervated by different neurons. (4) The iridescence neural circuit has a relay in the peripheral stellate ganglia. (5) The rise and decline of iridescence is much slower than that of chromatophores and can be elicited by light intensity changes.
References
DeMartini DG, Krogstad DV, Morse DE. 2013. Membrane invaginations facilitate reversible water flux driving tunable iridescence in a dynamic biophotonic system. P Natl Acad Sci USA. doi: 10.1073/pnas.1217260110
Izumi M, Sweeney AM, DeMartini D, Weaver JC, Powers ML, Tao A, Silvas TV, Kramer RM, Crookes-Goodson WJ, Mäthger LM, Naik RR, Hanlon RT, Morse DE. 2010. Changes in reflectin protein phosphorylation are associated with dynamic iridescence in squid. J R Soc Interface 7: 549-60. doi: 10.1098/rsif.2009.0299
Tao AR, DeMartini DG, Izumi M, Sweeney AM, Holt AL, Morse DE. 2010. The role of protein assembly in dynamically tunable bio-optical tissues. Biomaterials 31: 793-801. doi: 10.1016/j.biomaterials.2009.10.038
Wardill TJ, Gonzalez-Bellido PT, Crook RJ, Hanlon RT. 2012. Neural control of tuneable skin iridescence in squid. Proc. Roy. Soc. B 279: 4243-52. doi: 10.1098/rspb.2012.1374
Keywords:
Structural coloration,
Neural Stimulation,
skin patterning,
Stellate Ganglion,
Camouflage
Conference:
International Conference on Invertebrate Vision, Fjälkinge, Sweden, 1 Aug - 8 Aug, 2013.
Presentation Type:
Poster presentation preferred
Topic:
Colour and polarisation vision
Citation:
Wardill
TJ,
Gonzalez-Bellido
PT,
Crook
RJ and
Hanlon
RT
(2019). Luminance control of neurally tuneable skin iridescence in squid.
Front. Physiol.
Conference Abstract:
International Conference on Invertebrate Vision.
doi: 10.3389/conf.fphys.2013.25.00056
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Received:
23 Apr 2013;
Published Online:
09 Dec 2019.
*
Correspondence:
Dr. Trevor J Wardill, Marine Biological Laboratory, Program in Sensory Physiology and Behavior, Woods Hole, MA, 02543, United States, twardill@umn.edu
Dr. Paloma T Gonzalez-Bellido, Marine Biological Laboratory, Program in Sensory Physiology and Behavior, Woods Hole, MA, 02543, United States, paloma@mbl.edu