- Email: [email protected]
Animal Eyes: Filtering Out the Background
Current Biology
Dispatches 4. Gawryluk, R.M.R., Tikhonenkov, D.V., Hehenberger, E., Husnik, F., Mylnikov, A.P., and Keeling, P.J. (2019). Non-photosynthetic predators are sister to red algae. Nature 572, 240–243. 5. Klein, R.M., and Cronquist, A. (1967). A consideration of the evolutionary and taxonomic significance of some biochemical, micromorphological, and physiological characters in the thallophytes. Q. Rev. Biol. 42, 108–296. 6. Klein, R.M. (1970). Relationships between blue-green and red algae. Ann. N.Y. Acad. Sci. 17, 623–633. 7. Qiu, H., Price, D.C., Yang, E.C., Yoon, H.S., and Bhattacharya, D. (2015). Evidence of ancient genome reduction in red algae (Rhodophyta). J. Phycol. 51, 624–636. 8. Rossoni, A.W., Price, D.C., Seger, M., Lyska, D., Lammers, P., Bhattacharya, D., and Weber, A.P. (2019). The genomes of polyextremophilic cyanidiales contain 1% horizontally transferred genes with diverse adaptive functions. Elife 8, e45017.
9. Eichinger, L., Pachebat, J.A., Glo¨ckner, G., Rajandream, M.-A., Sucgang, R., Berriman, M., Song, J., Olsen, R., Szafranski, K., Xu, Q., et al. (2005). The genome of the social amoeba Dictyostelium discoideum. Nature 435, 43–57. 10. Fritz-Laylin, L.K., Prochnik, S.E., Ginger, M.L., Dacks, J.B., Carpenter, M.L., Field, M.C., Kuo, A., Paredez, A., Chapman, J., Pham, J., et al. (2010). The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140, 631–642. 11. Brawley, S.H., Blouin, N.A., Ficko-Blean, E., Wheeler, G.L., Lohr, M., Goodson, H.V., Jenkins, J.W., Blaby-Haas, C.E., Helliwell, K.E., Chan, C.X., et al. (2017). Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta). Proc. Natl. Acad. Sci. USA 114, E6361–E6370. 12. Archibald, J.M. (2015). Endosymbiosis and eukaryotic cell evolution. Curr. Biol. 25, R911–R921. 13. Gould, S.B., Waller, R.F., and McFadden, G.I. (2008). Plastid evolution. Annu. Rev. Plant Biol. 59, 491–517.
14. Smith, D.R., and Lee, R.W. (2014). A plastid without a genome: Evidence from the nonphotosynthetic green algal genus Polytomella. Plant Physiol. 164, 1812– 1819. 15. Ferna´ndez Robledo, J.A., Caler, E., Matsuzaki, M., Keeling, P.J., Shanmugam, D., Roos, D.S., and Vasta, G.R. (2011). The search for the missing link: A relic plastid in Perkinsus? Int. J. Parasitol. 41, 1217–1229. 16. Ralph, S.A., van Dooren, G.G., Waller, R.F., Crawford, M.J., Fraunholz, M.J., Foth, B.J., Tonkin, C.J., Roos, D.S., and McFadden, G.I. (2004). Tropical infectious diseases: Metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat. Rev. Microbiol. 2, 203–216. 17. de Koning, A., and Keeling, P. (2004). Nucleusencoded genes for plastid-targeted proteins in Helicosporidium: Functional diversity of a cryptic plastid in a parasitic alga. Eukaryot. Cell 3, 1198–1205. 18. Spiegel, F. (2012). Contemplating the first plantae. Science 335, 809–810. 19. Maruyama, S., and Kim, E. (2013). A modern descendant of early green algal phagotrophs. Curr. Biol. 23, 1081–1084.
Animal Eyes: Filtering Out the Background Venkata Jayasurya Yallapragada1 and Benjamin A. Palmer2,* 1Department
of Physics of Complex Systems, Weizmann Institute of Science, Rehovot, 7610001, Israel of Chemistry and The Ilse Katz Institute for Nanoscale Science and Technology, Ben-Gurion University of the Negev, Beer-Sheva, 8410501, Israel *Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.08.035 2Department
Animals use photonic structures in their eyes to form images, enhance sensitivity and provide camouflage. A recent exciting discovery shows that the eyes of some larval mantis shrimp possess photonic crystals that function as color filters to detect bioluminescence.
The animal kingdom is replete with spectacular manifestations of light reflection. Highly reflective materials such as silver and aluminium, which are ubiquitous in man-made mirrors, are not utilized by organisms. In animals, reflectivity is produced by the interference of light with structures exhibiting nanoscale variations in refractive index. Over 500 million years of evolution, the selective pressures of sex, camouflage and vision have resulted in the development of ingenious reflective structures, which enable animals to control the intensity and color of
reflected light. Iridescent, narrow-band colors are produced by highly-periodic structures [1], matte non-iridescent colors by partially ordered structures [2] and white coloration by light-scattering from randomly arranged objects of size comparable to optical wavelengths [3]. The best-known use for reflectivity in animals is in the production of structural coloration. The conspicuous colors of butterflies [4], peacocks [5], beetles [6] and tropical fish [7] have understandably been the subject of intensive study. However, it is in animal eyes that reflective optics have been
R938 Current Biology 29, R918–R941, October 7, 2019 ª 2019 Elsevier Ltd.
harnessed for the most extraordinary variety of biological functions [8], including image formation, enhancing photon capture, light barriers and camouflage (Figure 1). A recent paper by Feller et al. in Current Biology [9] reports the discovery of a remarkable photonic structure in the eyes of larval stomatopod crustaceans, with an entirely novel visual function. The socalled Intrarhabdomal Structural Reflector (ISR) functions as a spectral filter, which may enhance the larva’s ability to detect bioluminescence.
Current Biology
Dispatches
Figure 1. Reflectors in animal eyes. (A) The concave-mirrored eyes of the pecten scallop, Pecten maximus (courtesy of Prof. Dan-Eric Nillson, Lund University). (B) The choroidal tapetum of a sharpnose sevengill shark, Heptranchias perlo, that underlies the retina (courtesy of Prof. Nicholas Roberts, University of Bristol). (C) The reflecting iris of a zebrafish, Danio rerio (courtesy of Dr. Dvir Gur, National Institutes of Health & Janelia Research Campus). (D) Blue eye-shine from the camouflage reflector in the eyes of a nannosquillid stomatopod larvae, unknown species (courtesy of Dr. Kathryn Feller, University of Cambridge). (E) Corneal iridescence in the eyes of a puffer fish (courtesy of Mr. Kay Burn Lim, Iconic Images, www.kayburn.blog). (F) Green/yellow reflectance from the Intrarhabdomal Structural Reflector (ISR) in a stomatopod larvae (same species shown in (E)) (courtesy of Dr. Kathryn Feller, University of Cambridge).
Reflectivity in Vision Perhaps the most ‘sophisticated’ visual function of reflectivity is image formation. Although rare, some aquatic animals utilize mirrors rather than lenses to produce images [10]. Much like a minute reflecting telescope, scallops form images by reflecting light off a concave mirror onto an overlying retina [11,12] (Figure 1A). The mirror is composed of thin square-shaped crystals of guanine that in one direction have an unusually high refractive index of 1.83 [13]. The reflecting superposition compound eye of decapod crustaceans also uses mirrors to form a single upright image on the retina [14,15]. In this case the reflecting crystals are composed of isoxanthopterin, which has an even higher refractive index of around 2.0 [15]. A key concern for nocturnal animals or for those inhabiting light-deprived environments is to maximize photon capture. The eyes of many of these animals have an intensityenhancing ‘tapetum’ — a reflective structure underlying the retina (Figure 1B). The tapetum reflects transmitted photons back to the retina, providing the retinal
cells with a second chance for photon absorption. Reflectors are also used as light barriers in the irises of fish and cephalopods, preventing unfocussed light from entering the eye [16] (Figure 1C). Another important use for reflectivity in eyes, not directly related to vision, is camouflage. For many crustacean larvae living in pelagic environments, being transparent is key to avoiding detection. Some larval crustaceans have thus developed reflective structures overlying their opaque eye pigments to reduce their visibility to passing foe [17] (Figure 1D). Similarly, the beautiful corneal iridescence displayed by many teleost and puffer fish is thought to reduce the conspicuousness of the dark underlying pupil [18] (Figure 1E). The Intrarhabdomal Structural Reflector Adult stomatopods or mantis shrimps are famous for their amazing abilities to club or pierce their prey with their forelimbs. Feller et al. have discovered that the eyes of some larval stomatopods have an ingenious capability in vision — spectral
filtering. Compared to adult mantis shrimps, whose eyes exhibit an extraordinarily complex array of visual adaptations [19], larval mantis shrimps were thought to have comparatively simple apposition eyes. Apposition compound eyes contain hundreds of hexagonally faceted eye units called ommatidia which extend from the cornea to the retina. Refractive optics channel light entering individual ommatidia onto the rhabdom — the photoreceptive unit of the crustacean retina. The rhabdom is a column of tightly packed, orthogonally aligned microvilli containing the photosensitive visual pigment (Figure 2). The microvilli project out from a ring of seven surrounding retinal cells. Feller et al. found that the retinas of a sub-group of stomatopod larvae, the nannosquillids, contain a unique adaptation — the Intrarhabdomal Structural Reflector (ISR, Figure 1F). The ISR is a barrel-shaped structure embedded within the rhabdoms, directly along the optical pathway. The ISR effectively divides the rhabdom and the seven retinal cells into a distal and proximal tier. Feller et al. used
Current Biology 29, R918–R941, October 7, 2019 R939
Current Biology
Dispatches
Figure 2. The rhabdom. Cryo-SEM image of part of a rhabdom in the eye of an adult crayfish, Cherax quadricarinatus, showing the orthogonally oriented microvilli which project from different retinal cells.
two-photon and transmission electron microscopy to determine that the ISR is composed of a three-dimensionally ordered lattice of membrane-bound spherical nanoparticles (ca. 150 nm in diameter) (Figure 2 of Feller paper). The ordered arrangement of the nanoparticles within the ISR led the authors to think that it may function as a photonic crystal — a structure exhibiting periodic variations in refractive index. When light propagates through a photonic crystal some wavelengths are reflected much more efficiently than others. Indeed, in vivo reflectance spectroscopy and photonic modelling showed that the ISR does function as a wavelength-selective reflector, producing a narrowband reflection in the yellow range (572 nm). Yellow light impinging on the ISR will thus be reflected back to the overlying distal tier of rhabdom and its associated retinal cells. Since the ISR has no absorbing pigment, non-reflected light will be transmitted to the underlying proximal rhabdom, providing a spectral contrast between the upper and lower tiers of the retina. The ISR is therefore in essence a filter. But what is this filter used for? The only source of yellow light in the stomatopod’s habitat is emitted from
shallow-dwelling bioluminescent organisms. The authors propose that the ISR functions to remove a narrow, yellow band of this bioluminescence from impinging on the proximal tier of the retina. Quantum catch calculations showed that reflectance from the ISR increases the proportion of bioluminescent photons captured by the distal tier relative to the proximal tier of the rhabdom. The resulting spectral contrast between the two retinal tiers provides a possible mechanism for increasing the contrast of bioluminescent light against the blue ambient background, which may aid in the detection of bioluminescent prey species. Other organisms also use colored filters around their photoreceptors to tune spectral sensitivity by transmitting specific wavelengths of light not absorbed by the filter [20]. However, the stomatopod ISR utilizes a novel mechanism to achieve this result, simultaneously acting as a structural reflector and a transmissive filter. There are still many unresolved questions relating to the structure and function of the ISR. Interestingly, the ISR was found in only one clade of the
R940 Current Biology 29, R918–R941, October 7, 2019
stomatopod family — the nannosquillids. It is not known why. Feller and co-workers suggest the presence or absence of the ISR in different stomatopod species may be related to their different predation strategies; behavioral studies are required to demonstrate this. Also, the chemical identity and consequently the refractive index of the ISR nanoparticles could not be determined. This information is necessary for accurately modelling reflection from the ISR. Furthermore, determining the nature of the visual pigments in the proximal and distal tiers of the retina would be required to fully appreciate the utility of the ISR to the stomatopod larvae. The ISR is one of many extraordinary photonic devices in nature which continue to fascinate us. It seems certain that many more such optical treasures will be discovered in the future, particularly in animal eyes. Importantly, Feller’s paper illustrates the utility of combining experiments with computational modelling to provide a comprehensive understanding of the optical properties of biological systems. As well as being of fundamental importance to our understanding of the world around us, natural photonic devices have the potential to inspire a new generation of bio-compatible organic optical materials. Applying new imaging modalities, diffraction techniques and computation to elucidate the chemical, structural and optical properties of natural photonic materials will enable this goal to be realized.
REFERENCES 1. Vukusic, P., and Sambles, J.R. (2003). Photonic structures in biology. Nature 424, 852–855. 2. Noh, H., Liew, S.F., Saranathan, V., Mochrie, S.G.J., Prum, R.O., Dufresne, E.R., and Cao, H. (2010). How noniridescent colors are generated by quasi-ordered structures of bird feathers. Adv. Mater. 22, 2871–2880. 3. Burresi, M., Cortese, L., Pattelli, L., Kolle, M., Vukusic, P., Wiersma, D.S., Steiner, U., and Vignolini, S. (2014). Bright-white beetle scales optimise multiple scattering of light. Sci. Rep. 4, 6075. 4. Vukusic, P., Sambles, J.R., Lawrence, C.R., and Wooton, R.J. (1999). Quantified interference and diffraction in single Morpho butterfly scales. Proc. R. Soc. B. 266, 1403– 1411.
Current Biology
Dispatches 5. Zi, J., Yu, X., Li, Y., Hu, X., Xu, C., Wang, X., Liu, X., and Fu, R. (2003). Coloration strategies in peacock feathers. Proc. Natl. Acad. Sci. USA 100, 12576–12578.
10. Wagner, H.-J., Douglas, R.H., Frank, T.M., Roberts, N.W., and Partridge, J.C. (2009). A novel vertebrate eye using both refractive and reflective optics. Curr. Biol. 19, 108–114.
6. Saego, A.E., Brady, P., Vigneron, J.P., and Schultz, T.D. (2008). Gold bugs and beyond: a review of iridescence and structural colour mechanisms in beetles (Coleoptera). J. R. Soc. Interface 6, S165–S184.
11. Palmer, B.A., Taylor, G.J., Brumfeld, V., Gur, D., Shemesh, M., Elad, N., Osherov, A., Oron, D., Weiner, S., and Addadi, L. (2017). The image-forming mirror in the eye of the scallop. Science 358, 1172–1175.
7. Gur, D., Palmer, B.A., Leshem, B., Oron, D., Fratzl, P., Weiner, S., and Addadi, L. (2015). The mechanism of color change in the Neon Tetra fish: a light-induced tunable photonic crystal array. Angew. Chem. Int. Edit. 54, 12426–12430.
12. Land, M.F. (1965). Image formation by a concave reflector in the eye of the scallop, Pecten maximus. J. Physiol. 179, 138–153.
8. Palmer, B.A., Gur, D., Weiner, S., Addadi, L., and Oron, D. (2018). The organic crystalline materials of vision: structure-function considerations from the nanometer to the millimeter scale. Adv. Mater. 30, 1800006. 9. Feller, K.D., Wilby, D., Jacucci, G., Vignolini, S., Mantell, J., Wardill, T.J., Cronin, T.W., and Roberts, N.W. (2019). Long-wavelength reflecting filters found in the larval retinas of one mantis shrimp family (Nannosquillidae). Curr. Biol. 29, 3101–3108.e4.
13. Hirsch, A., Palmer, B.A., Elad, N., Gur, D., Weiner, S., Addadi, L., Kronik, L., and Leiserowitz, L. (2017). Biologically controlled morphology and twinning in guanine crystals. Angew. Chem. Int. Ed. 56, 9420–9424. 14. Land, M.F. (1976). Superposition images are formed by reflection in the eyes of some oceanic decapod crustacea. Nature 263, 764–765. 15. Palmer, B.A., Hirsch, A., Brumfeld, V., Aflalo, E.D., Pinkas, I., Sagi, A., Rosenne, S., Oron, D., Leiserowitz, L., Kronik, L., et al. (2018). Optically functional isoxanthopterin crystals in
the mirrored eyes of decapod crustaceans. Proc. Natl. Acad. Sci. USA 115, 2299–2304. 16. Gur, D., Nicolas, J.-D., Brumfeld, V., Bar-Elli, O., Oron, D., and Levkowitz, G. (2018). The dual functional reflecting iris of the zebrafish. Adv. Sci. 5, 1800338. 17. Feller, K.D., and Cronin, T.W. (2014). Hiding opaque eyes in transparent organisms: a potential role for larval eyeshine in stomatopod crustaceans. J. Exp. Biol. 217, 3263–3273. 18. Lythgoe, J.N. (1975). The structure and function of iridescent corneas in teleost fishes. Proc. R. Soc. Lond. B 188, 437–457. 19. Thoen, H.H., How, M.J., Chiou, T.H., and Marshall, J. (2014). A different form of color vision in mantis shrimp. Science 343, 411–413. 20. Cronin, T.W., Bok, M.J., Marshall, N.J., and Caldwell, R.L. (2014). Filtering and polychromatic vision in mantis shrimps: themes in visible and ultraviolet vision. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130032.
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Dispatches 4. Gawryluk, R.M.R., Tikhonenkov, D.V., Hehenberger, E., Husnik, F., Mylnikov, A.P., and Keeling, P.J. (2019). Non-photosynthetic predators are sister to red algae. Nature 572, 240–243. 5. Klein, R.M., and Cronquist, A. (1967). A consideration of the evolutionary and taxonomic significance of some biochemical, micromorphological, and physiological characters in the thallophytes. Q. Rev. Biol. 42, 108–296. 6. Klein, R.M. (1970). Relationships between blue-green and red algae. Ann. N.Y. Acad. Sci. 17, 623–633. 7. Qiu, H., Price, D.C., Yang, E.C., Yoon, H.S., and Bhattacharya, D. (2015). Evidence of ancient genome reduction in red algae (Rhodophyta). J. Phycol. 51, 624–636. 8. Rossoni, A.W., Price, D.C., Seger, M., Lyska, D., Lammers, P., Bhattacharya, D., and Weber, A.P. (2019). The genomes of polyextremophilic cyanidiales contain 1% horizontally transferred genes with diverse adaptive functions. Elife 8, e45017.
9. Eichinger, L., Pachebat, J.A., Glo¨ckner, G., Rajandream, M.-A., Sucgang, R., Berriman, M., Song, J., Olsen, R., Szafranski, K., Xu, Q., et al. (2005). The genome of the social amoeba Dictyostelium discoideum. Nature 435, 43–57. 10. Fritz-Laylin, L.K., Prochnik, S.E., Ginger, M.L., Dacks, J.B., Carpenter, M.L., Field, M.C., Kuo, A., Paredez, A., Chapman, J., Pham, J., et al. (2010). The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140, 631–642. 11. Brawley, S.H., Blouin, N.A., Ficko-Blean, E., Wheeler, G.L., Lohr, M., Goodson, H.V., Jenkins, J.W., Blaby-Haas, C.E., Helliwell, K.E., Chan, C.X., et al. (2017). Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta). Proc. Natl. Acad. Sci. USA 114, E6361–E6370. 12. Archibald, J.M. (2015). Endosymbiosis and eukaryotic cell evolution. Curr. Biol. 25, R911–R921. 13. Gould, S.B., Waller, R.F., and McFadden, G.I. (2008). Plastid evolution. Annu. Rev. Plant Biol. 59, 491–517.
14. Smith, D.R., and Lee, R.W. (2014). A plastid without a genome: Evidence from the nonphotosynthetic green algal genus Polytomella. Plant Physiol. 164, 1812– 1819. 15. Ferna´ndez Robledo, J.A., Caler, E., Matsuzaki, M., Keeling, P.J., Shanmugam, D., Roos, D.S., and Vasta, G.R. (2011). The search for the missing link: A relic plastid in Perkinsus? Int. J. Parasitol. 41, 1217–1229. 16. Ralph, S.A., van Dooren, G.G., Waller, R.F., Crawford, M.J., Fraunholz, M.J., Foth, B.J., Tonkin, C.J., Roos, D.S., and McFadden, G.I. (2004). Tropical infectious diseases: Metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat. Rev. Microbiol. 2, 203–216. 17. de Koning, A., and Keeling, P. (2004). Nucleusencoded genes for plastid-targeted proteins in Helicosporidium: Functional diversity of a cryptic plastid in a parasitic alga. Eukaryot. Cell 3, 1198–1205. 18. Spiegel, F. (2012). Contemplating the first plantae. Science 335, 809–810. 19. Maruyama, S., and Kim, E. (2013). A modern descendant of early green algal phagotrophs. Curr. Biol. 23, 1081–1084.
Animal Eyes: Filtering Out the Background Venkata Jayasurya Yallapragada1 and Benjamin A. Palmer2,* 1Department
of Physics of Complex Systems, Weizmann Institute of Science, Rehovot, 7610001, Israel of Chemistry and The Ilse Katz Institute for Nanoscale Science and Technology, Ben-Gurion University of the Negev, Beer-Sheva, 8410501, Israel *Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.08.035 2Department
Animals use photonic structures in their eyes to form images, enhance sensitivity and provide camouflage. A recent exciting discovery shows that the eyes of some larval mantis shrimp possess photonic crystals that function as color filters to detect bioluminescence.
The animal kingdom is replete with spectacular manifestations of light reflection. Highly reflective materials such as silver and aluminium, which are ubiquitous in man-made mirrors, are not utilized by organisms. In animals, reflectivity is produced by the interference of light with structures exhibiting nanoscale variations in refractive index. Over 500 million years of evolution, the selective pressures of sex, camouflage and vision have resulted in the development of ingenious reflective structures, which enable animals to control the intensity and color of
reflected light. Iridescent, narrow-band colors are produced by highly-periodic structures [1], matte non-iridescent colors by partially ordered structures [2] and white coloration by light-scattering from randomly arranged objects of size comparable to optical wavelengths [3]. The best-known use for reflectivity in animals is in the production of structural coloration. The conspicuous colors of butterflies [4], peacocks [5], beetles [6] and tropical fish [7] have understandably been the subject of intensive study. However, it is in animal eyes that reflective optics have been
R938 Current Biology 29, R918–R941, October 7, 2019 ª 2019 Elsevier Ltd.
harnessed for the most extraordinary variety of biological functions [8], including image formation, enhancing photon capture, light barriers and camouflage (Figure 1). A recent paper by Feller et al. in Current Biology [9] reports the discovery of a remarkable photonic structure in the eyes of larval stomatopod crustaceans, with an entirely novel visual function. The socalled Intrarhabdomal Structural Reflector (ISR) functions as a spectral filter, which may enhance the larva’s ability to detect bioluminescence.
Current Biology
Dispatches
Figure 1. Reflectors in animal eyes. (A) The concave-mirrored eyes of the pecten scallop, Pecten maximus (courtesy of Prof. Dan-Eric Nillson, Lund University). (B) The choroidal tapetum of a sharpnose sevengill shark, Heptranchias perlo, that underlies the retina (courtesy of Prof. Nicholas Roberts, University of Bristol). (C) The reflecting iris of a zebrafish, Danio rerio (courtesy of Dr. Dvir Gur, National Institutes of Health & Janelia Research Campus). (D) Blue eye-shine from the camouflage reflector in the eyes of a nannosquillid stomatopod larvae, unknown species (courtesy of Dr. Kathryn Feller, University of Cambridge). (E) Corneal iridescence in the eyes of a puffer fish (courtesy of Mr. Kay Burn Lim, Iconic Images, www.kayburn.blog). (F) Green/yellow reflectance from the Intrarhabdomal Structural Reflector (ISR) in a stomatopod larvae (same species shown in (E)) (courtesy of Dr. Kathryn Feller, University of Cambridge).
Reflectivity in Vision Perhaps the most ‘sophisticated’ visual function of reflectivity is image formation. Although rare, some aquatic animals utilize mirrors rather than lenses to produce images [10]. Much like a minute reflecting telescope, scallops form images by reflecting light off a concave mirror onto an overlying retina [11,12] (Figure 1A). The mirror is composed of thin square-shaped crystals of guanine that in one direction have an unusually high refractive index of 1.83 [13]. The reflecting superposition compound eye of decapod crustaceans also uses mirrors to form a single upright image on the retina [14,15]. In this case the reflecting crystals are composed of isoxanthopterin, which has an even higher refractive index of around 2.0 [15]. A key concern for nocturnal animals or for those inhabiting light-deprived environments is to maximize photon capture. The eyes of many of these animals have an intensityenhancing ‘tapetum’ — a reflective structure underlying the retina (Figure 1B). The tapetum reflects transmitted photons back to the retina, providing the retinal
cells with a second chance for photon absorption. Reflectors are also used as light barriers in the irises of fish and cephalopods, preventing unfocussed light from entering the eye [16] (Figure 1C). Another important use for reflectivity in eyes, not directly related to vision, is camouflage. For many crustacean larvae living in pelagic environments, being transparent is key to avoiding detection. Some larval crustaceans have thus developed reflective structures overlying their opaque eye pigments to reduce their visibility to passing foe [17] (Figure 1D). Similarly, the beautiful corneal iridescence displayed by many teleost and puffer fish is thought to reduce the conspicuousness of the dark underlying pupil [18] (Figure 1E). The Intrarhabdomal Structural Reflector Adult stomatopods or mantis shrimps are famous for their amazing abilities to club or pierce their prey with their forelimbs. Feller et al. have discovered that the eyes of some larval stomatopods have an ingenious capability in vision — spectral
filtering. Compared to adult mantis shrimps, whose eyes exhibit an extraordinarily complex array of visual adaptations [19], larval mantis shrimps were thought to have comparatively simple apposition eyes. Apposition compound eyes contain hundreds of hexagonally faceted eye units called ommatidia which extend from the cornea to the retina. Refractive optics channel light entering individual ommatidia onto the rhabdom — the photoreceptive unit of the crustacean retina. The rhabdom is a column of tightly packed, orthogonally aligned microvilli containing the photosensitive visual pigment (Figure 2). The microvilli project out from a ring of seven surrounding retinal cells. Feller et al. found that the retinas of a sub-group of stomatopod larvae, the nannosquillids, contain a unique adaptation — the Intrarhabdomal Structural Reflector (ISR, Figure 1F). The ISR is a barrel-shaped structure embedded within the rhabdoms, directly along the optical pathway. The ISR effectively divides the rhabdom and the seven retinal cells into a distal and proximal tier. Feller et al. used
Current Biology 29, R918–R941, October 7, 2019 R939
Current Biology
Dispatches
Figure 2. The rhabdom. Cryo-SEM image of part of a rhabdom in the eye of an adult crayfish, Cherax quadricarinatus, showing the orthogonally oriented microvilli which project from different retinal cells.
two-photon and transmission electron microscopy to determine that the ISR is composed of a three-dimensionally ordered lattice of membrane-bound spherical nanoparticles (ca. 150 nm in diameter) (Figure 2 of Feller paper). The ordered arrangement of the nanoparticles within the ISR led the authors to think that it may function as a photonic crystal — a structure exhibiting periodic variations in refractive index. When light propagates through a photonic crystal some wavelengths are reflected much more efficiently than others. Indeed, in vivo reflectance spectroscopy and photonic modelling showed that the ISR does function as a wavelength-selective reflector, producing a narrowband reflection in the yellow range (572 nm). Yellow light impinging on the ISR will thus be reflected back to the overlying distal tier of rhabdom and its associated retinal cells. Since the ISR has no absorbing pigment, non-reflected light will be transmitted to the underlying proximal rhabdom, providing a spectral contrast between the upper and lower tiers of the retina. The ISR is therefore in essence a filter. But what is this filter used for? The only source of yellow light in the stomatopod’s habitat is emitted from
shallow-dwelling bioluminescent organisms. The authors propose that the ISR functions to remove a narrow, yellow band of this bioluminescence from impinging on the proximal tier of the retina. Quantum catch calculations showed that reflectance from the ISR increases the proportion of bioluminescent photons captured by the distal tier relative to the proximal tier of the rhabdom. The resulting spectral contrast between the two retinal tiers provides a possible mechanism for increasing the contrast of bioluminescent light against the blue ambient background, which may aid in the detection of bioluminescent prey species. Other organisms also use colored filters around their photoreceptors to tune spectral sensitivity by transmitting specific wavelengths of light not absorbed by the filter [20]. However, the stomatopod ISR utilizes a novel mechanism to achieve this result, simultaneously acting as a structural reflector and a transmissive filter. There are still many unresolved questions relating to the structure and function of the ISR. Interestingly, the ISR was found in only one clade of the
R940 Current Biology 29, R918–R941, October 7, 2019
stomatopod family — the nannosquillids. It is not known why. Feller and co-workers suggest the presence or absence of the ISR in different stomatopod species may be related to their different predation strategies; behavioral studies are required to demonstrate this. Also, the chemical identity and consequently the refractive index of the ISR nanoparticles could not be determined. This information is necessary for accurately modelling reflection from the ISR. Furthermore, determining the nature of the visual pigments in the proximal and distal tiers of the retina would be required to fully appreciate the utility of the ISR to the stomatopod larvae. The ISR is one of many extraordinary photonic devices in nature which continue to fascinate us. It seems certain that many more such optical treasures will be discovered in the future, particularly in animal eyes. Importantly, Feller’s paper illustrates the utility of combining experiments with computational modelling to provide a comprehensive understanding of the optical properties of biological systems. As well as being of fundamental importance to our understanding of the world around us, natural photonic devices have the potential to inspire a new generation of bio-compatible organic optical materials. Applying new imaging modalities, diffraction techniques and computation to elucidate the chemical, structural and optical properties of natural photonic materials will enable this goal to be realized.
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