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Organisms appear opaque largely because their outer tissue layers are strongly scattering to incident light; strongly absorbing pigments, such as blood, typically have narrow absorbances, such that the mean free path of light outside the absorbance peaks can be quite long. As people cannot see through tissue, they generally imagine that tissues like the brain, fat, and bone contain little or no light. However, photoresponsive opsin proteins are expressed within many of these tissues, and their functions are poorly understood. Radiance internal to tissue is also important for understanding photosynthesis. For example, giant clams are strongly absorbing yet maintain a dense population of algae deep in the tissue. Light propagation through systems like sediments and biofilms can be complex, and these communities can be major contributors to ecosystem productivity. Therefore, a method for constructing optical micro-probes for measuring scalar irradiance (photon flux intersecting a point) and downwelling irradiance (photon flux crossing a plane perpendicularly) to better understand these phenomena inside living tissue has been developed. This technique is also tractable in field laboratories. These micro-probes are made from heat-pulled optical fibers that are then secured in pulled glass pipettes. To change the angular acceptance of the probe, a 10-100 µm sized sphere of UV-curable epoxy mixed with titanium dioxide is then secured to the end of a pulled, trimmed fiber. The probe is inserted into living tissue, and its position is controlled using a micromanipulator. These probes are capable of measuring in situ tissue radiance at spatial resolutions of 10-100 µm or on the scale of single cells. These probes were used to characterize the light reaching the adipose and brain cells 4 mm below the skin of a living mouse and to characterize the light reaching similar depths within living algae-rich giant clam tissue.

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Squids have spherical, gradient index lenses that maximize optical sensitivity while minimizing light scattering and geometric aberration. Previous studies have shown that the constituent lens proteins behave like patchy particles, and that a density gradient of packing fraction ∼0.01 to 1 assembles from a gradient of average particle valence, 〈M〉 ≈ 2.1 to 〈M〉 > 6. A priori, transparency requires that all regions within the larger gradient must minimize density fluctuations at length scales close to the wavelength of visible light. It is not known how a material can achieve this at all possible packing fractions via attractive interactions. We also observe that the set of proteins making the lens is remarkably polydisperse (there are around 40 isoforms expressed). Why does nature employ so many geometrically similar isoforms when theory suggests a few would suffice, and what, if any, is the physical role of the polydispersity? This study focuses on answering these questions for the sparsest regions of the lens, where the patchy nature of the system will have the largest influence on the final structure. We first simulated mixtures of bi- and trivalent patchy particles and found a strong influence of patch angle on the percolation and gel structure of the system. We then investigated the influence of the interaction polydispersity on the structure of the M = 2.1 system. We find that increasing the variance in patch energies and single-patch angle appears to decrease the length scale of density fluctuations while also moving the percolation line to lower temperature. S-Crystallin geometry and polydispersity appear to promote regular percolation of a gel structure while also limiting density fluctuations to small length scales, thereby promoting transparency in the annealed structure.

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Sponges are animals that inhabit many aquatic environments while filtering small particles and ejecting metabolic wastes. They are composed of cells in a bulk extracellular matrix, often with an embedded scaffolding of stiff, siliceous spicules. We hypothesize that the mechanical response of this heterogeneous tissue to hydrodynamic flow influences cell proliferation in a manner that generates the body of a sponge. Towards a more complete picture of the emergence of sponge morphology, we dissected a set of species and subjected discs of living tissue to physiological shear and uniaxial deformations on a rheometer. Various species exhibited rheological properties such as anisotropic elasticity, shear softening and compression stiffening, negative normal stress, and non-monotonic dissipation as a function of both shear strain and frequency. Erect sponges possessed aligned, spicule-reinforced fibres which endowed three times greater stiffness axially compared with orthogonally. By contrast, tissue taken from shorter sponges was more isotropic but time-dependent, suggesting higher flow sensitivity in these compared with erect forms. We explore ecological and physiological implications of our results and speculate about flow-induced mechanical signalling in sponge cells.

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The ornately geometric walls of pollen grains have inspired scientists for decades. We show that the evolved diversity of these patterns is entirely recapitulated by a biophysical model in which an initially uniform polysaccharide layer in the extracellular space, mechanically coupled to the cell membrane, phase separates to a spatially modulated state. Experiments reveal this process occurring in living cells. We observe that in ∼10% of extant species, this phase separation reaches equilibrium during development such that individual pollen grains are identical and perfectly reproducible. About 90% of species undergo an arrest of this process prior to equilibrium such that individual grains are similar but inexact copies. Equilibrium patterns have appeared multiple times during the evolution of seed plants, but selection does not favor these states. This framework for pattern development provides a route to rationalizing the surface textures of other secreted structures, such as cell walls and insect cuticle.

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Ctenophores, or comb jellies, are among the earliest-diverging extant animal lineages. Several recent phylogenomic studies suggest that they may even be the sister group to all other animals. This unexpected finding remains difficult to contextualize, particularly given ctenophores' unique and sometimes poorly understood physiology. Colloblasts, a ctenophore-specific cell type found on the surface of these animals' tentacles, are emblematic of this difficulty. The exterior of the colloblast is dotted with granules that burst and release an adhesive on contact with prey, ensnaring it for consumption. To date, little is known about the fast-acting underwater adhesive that these cells secrete or its biochemistry. We present evidence that proteins in the colloblasts of the ctenophore Pleurobrachia bachei incorporate catecholic compounds similar to the amino acid l-3,4-dihydroxyphenylalanine. These compounds are associated with adhesive-containing granules on the surface of colloblasts, suggesting that they may play a role in prey capture, akin to dihydroxyphenylalanine-based adhesives in mussel byssus. We also present unexpected evidence of similar catecholic compounds in association with the subepithelial nerve net. There, catecholic compounds are present in spatial patterns similar to those of l-3,4-dihydroxyphenylalanine and its derivatives in cnidarian nerves, where they are associated with membranes and possess unknown functionality. This "structural" use of catecholic molecules in ctenophores represents the earliest-diverging animal lineage in which this trait has been observed, though it remains unclear whether structural catechols are deeply rooted in animals or whether they have arisen multiple times.

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The Chinese century egg, or pidan, is a traditional preparation of duck eggs that can be stored for months at room temperature without degradation. Raw eggs are soaked in a strong alkaline and salt solution, and the albumin gradually forms a stable, transparent gel. Here, we show that pidan gels belong to the class of materials formed from "patchy particles". We found that the ß-sheet structure of ovalbumin, the major protein constituent of egg white, is preserved during gelation, while α-helical regions undergo a degree of unfolding into unstructured random coils that may form attractive patches. Upon dilution in additional strong base, the phase behavior of pidan gels is consistent with patchy-particle thermodynamics. This protein gel is also physically and structurally similar to the protein gels that form the squid lens. Both systems exhibit patchy thermodynamics, and the constituent proteins share physical features including a structured, charged core, and polar, unstructured "arms" that form attractive patches. Our work provides a path toward rational design of proteins for precisely structured, volume-spanning materials.

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This corrects the article DOI: 10.1038/srep26756.

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It will be ideal to deliver equal, optimally efficient "doses" of sunlight to all cells in a photobioreactor system, while simultaneously utilizing the entire solar resource. Backed by the numerical scattering simulation and optimization, here, the design, synthesis, and characterization of the synthetic iridocytes that recapitulated the salient forward-scattering behavior of the Tridacnid clam system are reported, which presents the first geometric solution to allow narrow, precise forward redistribution of flux, utilizing the solar resource at the maximum quantum efficiency possible in living cells. The synthetic iridocytes are composed of silica nanoparticles in microspheres embedded in gelatin, both are low refractive index materials and inexpensive. They show wavelength selectivity, have little loss (the back-scattering intensity is reduced to less than ≈0.01% of the forward-scattered intensity), and narrow forward scattering cone similar to giant clams. Moreover, by comparing experiments and theoretical calculation, it is confirmed that the nonuniformity of the scatter sizes is a "feature not a bug" of the design, allowing for efficient, forward redistribution of solar flux in a micrometer-scaled paradigm. This method is environmentally benign, inexpensive, and scalable to produce optical components that will find uses in efficiency-limited solar conversion technologies, heat sinks, and biofuel production.

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The largest habitat by volume on Earth is the oceanic midwater, which is also one of the least understood in terms of animal ecology. The organisms here exhibit a spectacular array of optical adaptations for living in a visual void that have only barely begun to be described. We describe a complex pattern of broadband scattering from the skin of Argyropelecus sp., a hatchetfish found in the mesopelagic zone of the world's oceans. Hatchetfish skin superficially resembles the unpolished side of aluminium foil, but on closer inspection contains a complex composite array of subwavelength-scale dielectric structures. The superficial layer of this array contains dielectric stacks that are rectangular in cross-section, while the deeper layer contains dielectric bundles that are elliptical in cross-section; the cells in both layers have their longest dimension running parallel to the dorsal-ventral axis of the fish. Using the finite-difference time-domain approach and photographic radiometry, we explored the structural origins of this scattering behaviour and its environmental consequences. When the fish's flank is illuminated from an arbitrary incident angle, a portion of the scattered light exits in an arc parallel to the fish's anterior-posterior axis. Simultaneously, some incident light is also scattered downwards through the complex birefringent skin structure and exits from the ventral photophores. We show that this complex scattering pattern will provide camouflage simultaneously against the horizontal radially symmetric solar radiance in this habitat, and the predatory bioluminescent searchlights that are common here. The structure also directs light incident on the flank of the fish into the downwelling, silhouette-hiding counter-illumination of the ventral photophores.

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Galiteuthis, a midwater squid, has photophores on the ventral surfaces of its eyes. These photophores emit bioluminescence to counter-illuminate the shadows cast by the eyes in downwelling sunlight, thereby hiding the eyes from upward-looking predators. The photophores consist of laminated fibre-like cells with semi-coaxial protein-dense layers around axial cytoplasm. These cells have been suggested to function as light guides: bioluminescence is an isotropic process used to hide in an anisotropic light environment, so any emission must be reshaped to be effective. We found a wide variation in cross-sectional geometries of photophore cells; some were more efficient at light guiding than others. We used a set of optical models to place these photophores in the context of the radiance where Galiteuthis lives and discovered a possible adaptive reason for this variation. In Galiteuthis's horizontal and vertical range, ocean radiance is also quite variable. For complete camouflage, photophores must reproduce this variation in radiance using an isotropic source. Our models show that variation in the geometry of the photophore light guides reproduces the predicted variation in ocean radiance experienced by this species. By selectively activating geometrically distinct populations of photophore cells, the animal may reproduce the angular distribution of light at all positions in its habitat.

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The illumination of the environment undergoes both intensity and spectral changes during the 24 h cycle of a day. Daylight spectral power distributions are well described by low-dimensional models such as the CIE (Commission Internationale de l'Éclairage) daylight model, but the performance of this model in non-daylight regimes is not characterised. We measured downwelling spectral irradiance across multiple days in two locations in North America: One rural location (Cherry Springs State Park, PA) with minimal anthropogenic light sources, and one city location (Philadelphia, PA). We characterise the spectral, intensity and colour changes and extend the existing CIE model for daylight to capture twilight components and the spectrum of the night sky.

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We propose a general theory for surface patterning in many different biological systems, including mite and insect cuticles, pollen grains, fungal spores, and insect eggs. The patterns of interest are often intricate and diverse, yet an individual pattern is robustly reproducible by a single species and a similar set of developmental stages produces a variety of patterns. We argue that the pattern diversity and reproducibility may be explained by interpreting the pattern development as a first-order phase transition to a spatially modulated phase. Brazovskii showed that for such transitions on a flat, infinite sheet, the patterns are uniform striped or hexagonal. Biological objects, however, have finite extent and offer different topologies, such as the spherical surfaces of pollen grains. We consider Brazovskii transitions on spheres and show that the patterns have a richer phenomenology than simple stripes or hexagons. We calculate the free energy difference between the unpatterned state and the many possible patterned phases, taking into account fluctuations and the system's finite size. The proliferation of variety on a sphere may be understood as a consequence of topology, which forces defects into perfectly ordered phases. The defects are then accommodated in different ways. We also argue that the first-order character of the transition is responsible for the reproducibility and robustness of the pattern formation.

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'Giant' tridacnid clams have evolved a three-dimensional, spatially efficient, photodamage-preventing system for photosymbiosis. We discovered that the mantle tissue of giant clams, which harbours symbiotic nutrition-providing microalgae, contains a layer of iridescent cells called iridocytes that serve to distribute photosynthetically productive wavelengths by lateral and forward-scattering of light into the tissue while back-reflecting non-productive wavelengths with a Bragg mirror. The wavelength- and angle-dependent scattering from the iridocytes is geometrically coupled to the vertically pillared microalgae, resulting in an even re-distribution of the incoming light along the sides of the pillars, thus enabling photosynthesis deep in the tissue. There is a physical analogy between the evolved function of the clam system and an electric transformer, which changes energy flux per area in a system while conserving total energy. At incident light levels found on shallow coral reefs, this arrangement may allow algae within the clam system to both efficiently use all incident solar energy and avoid the photodamage and efficiency losses due to non-photochemical quenching that occur in the reef-building coral photosymbiosis. Both intra-tissue radiometry and multiscale optical modelling support our interpretation of the system's photophysics. This highly evolved 'three-dimensional' biophotonic system suggests a strategy for more efficient, damage-resistant photovoltaic materials and more spatially efficient solar production of algal biofuels, foods and chemicals.

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Photonic structures in the skin of pelagic fishes and squids evolved specifically for hiding in the complex light field of the open ocean. To understand the principles under which these structures operate, a detailed characterization of their optical properties is required. An optical scatterometer has been developed to measure one important property, the bidirectional reflectance distribution function (BRDF). The instrument was used to collect reflectance functions from the squid Pterygioteuthis microlampas and fish Sternoptyx sp. Although the animals appear very different to a casual observer, the results reveal interesting similarities in their scattering patterns, suggesting a similar optical strategy for hiding in open water.

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Synchrony of spawning in many hermatypic corals, typically a few nights after the full moon, is putatively dependent on solar and lunar light cycles in conjunction with other possible cues such as tides and temperature. We analyze here the contributions of separate components of light dynamics, because the effects of twilight and lunar skylight on coral spawning synchrony have previously been conflated and the alternative hypothesis that these components have differential contributions as proximate cues has not been tested. Moonlight-dependent changes in spectra during twilight, rates of decreasing twilight intensities, and changes in lunar photoperiod were experimentally decoupled using programmed light-emitting diodes and compared for their separate effects on spawning synchrony in Acropora humilis. Effects on synchrony under the control of synthetic lunar cues were greatest in response to changes in lunar photoperiod; changes in light intensities and spectra had lesser influence. No significant differences among treatment responses were found at the circa-diel time scale. We conclude that spawning synchrony on a particular lunar night and specific time of night is a threshold response to differential periods of darkness after twilight that is primarily influenced by lunar photoperiod and secondarily by discrete optical components of early nocturnal illumination.

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Cephalopods possess a sophisticated array of mechanisms to achieve camouflage in dynamic underwater environments. While active mechanisms such as chromatophore patterning and body posturing are well known, passive mechanisms such as manipulating light with highly evolved reflectors may also play an important role. To explore the contribution of passive mechanisms to cephalopod camouflage, we investigated the optical and biochemical properties of the silver layer covering the eye of the California fishery squid, Loligo opalescens. We discovered a novel nested-spindle geometry whose correlated structure effectively emulates a randomly distributed Bragg reflector (DBR), with a range of spatial frequencies resulting in broadband visible reflectance, making it a nearly ideal passive camouflage material for the depth at which these animals live. We used the transfer-matrix method of optical modelling to investigate specular reflection from the spindle structures, demonstrating that a DBR with widely distributed thickness variations of high refractive index elements is sufficient to yield broadband reflectance over visible wavelengths, and that unlike DBRs with one or a few spatial frequencies, this broadband reflectance occurs from a wide range of viewing angles. The spindle shape of the cells may facilitate self-assembly of a random DBR to achieve smooth spatial distributions in refractive indices. This design lends itself to technological imitation to achieve a DBR with wide range of smoothly varying layer thicknesses in a facile, inexpensive manner.

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There are dramatic and physiologically relevant changes in both skylight color and intensity during evening twilight as the pathlength of direct sunlight through the atmosphere increases, ozone increasingly absorbs long wavelengths and skylight becomes increasingly blue shifted. The moon is above the horizon at sunset during the waxing phase of the lunar cycle, on the horizon at sunset on the night of the full moon and below the horizon during the waning phase. Moonlight is red shifted compared with daylight, so the presence, phase and position of the moon in the sky could modulate the blue shifts during twilight. Therefore, the influence of the moon on twilight color is likely to differ somewhat each night of the lunar cycle, and to vary especially rapidly around the full moon, as the moon transitions from above to below the horizon during twilight. Many important light-mediated biological processes occur during twilight, and this lunar effect may play a role. One particularly intriguing biological event tightly correlated with these twilight processes is the occurrence of mass spawning events on coral reefs. Therefore, we measured downwelling underwater hyperspectral irradiance on a coral reef during twilight for several nights before and after the full moon. We demonstrate that shifts in twilight color and intensity on nights both within and between evenings, immediately before and after the full moon, are correlated with the observed times of synchronized mass spawning, and that these optical phenomena are a biologically plausible cue for the synchronization of these mass spawning events.

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Cephalopods are nicknamed the "masters of disguise" for their highly evolved camouflage mechanisms, including the hallmark ability to rapidly change the color and reflectance of their skin. Previously, reflectin proteins were identified as the major biomaterial component of iridosomes [1], specialized light-reflecting architectures that contribute intense structural color to squid skin, eyes, and organs [2-5]. Supramolecular assembly of reflectin has been recognized as a key property in the protein's function [6]. Here, we report the first cloning and expression of a specific reflectin protein found in the responsive iridophore cells of the squid Loligo pealeii, which are unique in their ability to switch on/off and change color. We demonstrate that these iridophores can be chemically tuned to reflect the entire visible spectrum. By examining recombinant reflectin, we show that this dynamic optical function is facilitated by the hierarchical assembly of nanoscale protein particles that elicit large volume changes upon condensation. These findings provide insight into the design and synthesis of biomaterials for complex, responsive function in optical applications.

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Many cephalopods exhibit remarkable dermal iridescence, a component of their complex, dynamic camouflage and communication. In the species Euprymna scolopes, the light-organ iridescence is static and is due to reflectin protein-based platelets assembled into lamellar thin-film reflectors called iridosomes, contained within iridescent cells called iridocytes. Squid in the family Loliginidae appear to be unique in which the dermis possesses a dynamic iridescent component with reflective, coloured structures that are assembled and disassembled under the control of the muscarinic cholinergic system and the associated neurotransmitter acetylcholine (ACh). Here we present the sequences and characterization of three new members of the reflectin family associated with the dynamically changeable iridescence in Loligo and not found in static Euprymna iridophores. In addition, we show that application of genistein, a protein tyrosine kinase inhibitor, suppresses ACh- and calcium-induced iridescence in Loligo. We further demonstrate that two of these novel reflectins are extensively phosphorylated in concert with the activation of iridescence by exogenous ACh. This phosphorylation and the correlated iridescence can be blocked with genistein. Our results suggest that tyrosine phosphorylation of reflectin proteins is involved in the regulation of dynamic iridescence in Loligo.

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A lens with a graded refractive index is required for vision in aquatic animals with camera-type eyes. This optical design entails a radial gradient of protein density, with low density in external layers and high density in internal layers. To maintain the optical stability of the eye, different material properties are required for proteins in different regions of the lens. In low-density regions of the lens where slight protein aggregation causes significant light scattering, aggregation must be minimized. Squid lens S-crystallin proteins are evolutionarily derived from the glutathione S-transferase protein family. We used biochemistry, optical modelling and phylogenetics to study the evolution and material properties of S-crystallins. S-crystallins are differentially expressed in a radial gradient, suggesting a role in refractive index. This gradient in S-crystallin expression is correlated with their evolutionary history and biochemistry. S-crystallins have been under positive selection. This selection appears to have resulted in stabilization of derived S-crystallins via mutations in the dimer interface and extended electrostatic fields. These derived S-crystallins probably cause the glassy organization and stability of low refractive index lens layers. Our work elucidates the molecular and evolutionary mechanisms underlying the production and maintenance of camera-like optics in squid lenses.

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