Development of High-Order Organization of Guanine-Based Reflectors Underlies the Dual Functionality of the Zebrafish Iris

Many marine organisms have evolved a reflective iris to prevent unfocused light from reaching the retina. The fish iris has a dual function, both to camouflage the eye and serving as a light barrier. Yet, the mechanism that enables this dual functionality and the benefits of using a reflective iris have remained unclear. Using synchrotron micro-focused diffraction, cryo-SEM imaging and optical analyses on zebrafish at different stages of development, we show that the complex optical response of the iris is facilitated by the development a high-order organization of multilayered guanine-based crystal reflectors and pigments. We further demonstrates how the efficient light reflector is established during development to allow the optical functionality of the eye, already at early developmental stages. These results shed light on the evolutionary drive for developing a compact reflective iris, which are widely used by many animal species. One Sentence Summary The dual function of the zebrafish iris as a light barrier and camouflage reflector is enabled by the high-order organization of intracellular guanine crystals and pigments.

[1]  S. Weiner,et al.  Structural Basis for the Brilliant Colors of the Sapphirinid Copepods. , 2015, Journal of the American Chemical Society.

[2]  Hime,et al.  Fishes with Eye Shine : Functional Morphology of Guanine Type Tapetum Lucidum , 2006 .

[3]  E. Denton,et al.  Review lecture: on the organization of reflecting surfaces in some marine animals. , 1970, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[4]  C. Nüsslein-Volhard,et al.  Gap junctions composed of connexins 41.8 and 39.4 are essential for colour pattern formation in zebrafish , 2014, eLife.

[5]  H. Haberman,et al.  A qualitative study of the melanins from blue and brown human eyes. , 1982, Experimental eye research.

[6]  Shigeru Kondo,et al.  Pigment cell distributions in different tissues of the zebrafish, with special reference to the striped pigment pattern , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[7]  L. Addadi,et al.  “Guanigma”: The Revised Structure of Biogenic Anhydrous Guanine , 2015 .

[8]  M F Land,et al.  Mechanism of reflexion in silvery layers of fish and cephalopods , 1971, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[9]  S. Weiner,et al.  The structural basis for enhanced silver reflectance in Koi fish scale and skin. , 2014, Journal of the American Chemical Society.

[10]  S. Neuhauss,et al.  Visual behavior in zebrafish. , 2006, Zebrafish.

[11]  S. Johnsen,et al.  The Optics of Life: A Biologist's Guide to Light in Nature , 2012 .

[12]  G. K. Smelser The Vertebrate Eye and Its Adaptive Radiation. , 1943 .

[13]  Valery V. Tuchin,et al.  Estimation of melanin content in iris of human eye , 2005, SPIE BiOS.

[14]  D. M. Allen,et al.  Peripheral Rods Evade Light Damage in Albino Trout , 2001 .

[15]  S. A. Talbot Physiology of the retina and the visual pathway , 1961 .

[16]  S. Neuhauss Zebrafish vision: Structure and function of the zebrafish visual system , 2010 .

[17]  M. Burghammer,et al.  Scanning X-ray diffraction on cardiac tissue: automatized data analysis and processing. , 2017, Journal of synchrotron radiation.

[18]  C. Hawryshyn,et al.  Visual pigment composition in zebrafish: Evidence for a rhodopsin–porphyropsin interchange system , 2004, Visual Neuroscience.

[19]  B. Link,et al.  Morphogenesis of the anterior segment in the zebrafish eye , 2005, BMC Developmental Biology.

[20]  Shigeru Kondo,et al.  Pigment Pattern Formation by Contact-Dependent Depolarization , 2012, Science.

[21]  Richard S. Smith,et al.  The aqueous humor outflow pathway of zebrafish. , 2009, Investigative ophthalmology & visual science.

[22]  S. Weiner,et al.  The mechanism of color change in the neon tetra fish: a light-induced tunable photonic crystal array. , 2015, Angewandte Chemie.

[23]  D. Parichy,et al.  Long-distance communication by specialized cellular projections during pigment pattern development and evolution , 2015, eLife.

[24]  S. Weiner,et al.  Guanine-based photonic crystals in fish scales form from an amorphous precursor. , 2013, Angewandte Chemie.

[25]  Masakatsu Watanabe,et al.  Involvement of Delta/Notch signaling in zebrafish adult pigment stripe patterning , 2014, Development.

[26]  S. Easter,et al.  The development of vision in the zebrafish (Danio rerio). , 1996, Developmental biology.

[27]  Tim Salditt,et al.  Anisotropic x-ray scattering and orientation fields in cardiac tissue cells , 2017 .

[28]  Timothy R. Parsons,et al.  Biological oceanography: an introduction. Second edition , 1997 .

[29]  J. Lythgoe,et al.  Changes in spectral reflexions from the iridophores of the neon tetra. , 1982, The Journal of physiology.

[30]  D. A. Cameron Mapping absorbance spectra, cone fractions, and neuronal mechanisms to photopic spectral sensitivity in the zebrafish. , 2002, Visual neuroscience.

[31]  J. Nicol,et al.  A survey of reflectivity in silvery teleosts , 1966, Journal of the Marine Biological Association of the United Kingdom.

[32]  G. L. Walls,et al.  The Vertebrate Eye and Its Adaptive Radiation. , 2013 .