Structural Diversity of Arthropod Biophotonic Nanostructures Spans

May 4, 2015 - Many organisms, especially arthropods, produce vivid interference colors using diverse mesoscopic (100–350 nm) integumentary biophoton...
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Structural Diversity of Arthropod Biophotonic Nanostructures Spans Amphiphilic Phase-Space Vinodkumar Saranathan,*,†,‡,⊥,¶ Ainsley E. Seago,§ Alec Sandy,∥ Suresh Narayanan,∥ Simon G. J. Mochrie,#,¶ Eric R. Dufresne,#,∇,○,¶ Hui Cao,#,∇,¶ Chinedum O. Osuji,◆,¶ and Richard O. Prum*,⊥,¶ †

Division of Physics and Applied Physics, School of Physical and Mathematical Sciences, Nanyang Technological University, 21 Nanyang Link, 637371, Singapore ‡ Edward Grey Institute of Field Ornithology, Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, United Kingdom § CSIRO Ecosystem Sciences, GPO Box 1700, Canberra, Australian Capital Territory 2601, Australia ∥ Advanced Photon Source, Argonne National Laboratory, Argonne, Illinois 60439, United States ⊥ Department of Ecology and Evolutionary Biology, and Peabody Museum of Natural History, #Department of Physics, ∇Department of Applied Physics, ○Department of Mechanical Engineering and Materials Science, ◆Department of Chemical and Environmental Engineering, and ¶Center for Research on Interface Structures and Phenomenon (CRISP), Yale University, New Haven, Connecticut 06520, United States S Supporting Information *

ABSTRACT: Many organisms, especially arthropods, produce vivid interference colors using diverse mesoscopic (100−350 nm) integumentary biophotonic nanostructures that are increasingly being investigated for technological applications. Despite a century of interest, precise structural knowledge of many biophotonic nanostructures and the mechanisms controlling their development remain tentative, when such knowledge can open novel biomimetic routes to facilely self-assemble tunable, multifunctional materials. Here, we use synchrotron small-angle X-ray scattering and electron microscopy to characterize the photonic nanostructure of 140 integumentary scales and setae from ∼127 species of terrestrial arthropods in 85 genera from 5 orders. We report a rich nanostructural diversity, including triply periodic bicontinuous networks, close-packed spheres, inverse columnar, perforated lamellar, and disordered spongelike morphologies, commonly observed as stable phases of amphiphilic surfactants, block copolymer, and lyotropic lipid−water systems. Diverse arthropod lineages appear to have independently evolved to utilize the self-assembly of infolding lipid-bilayer membranes to develop biophotonic nanostructures that span the phase-space of amphiphilic morphologies, but at optical length scales. KEYWORDS: Biophotonic nanostructures, structural colors, iridescence, self-assembly, membrane-folding, biomimetics

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In terrestrial arthropods, structural colors are often produced by the well-characterized class of one-dimensional biophotonic nanostructures comprising thin-film, lamellar (multilayer) reflectors, or diffraction gratings in the cuticle of the integument.2−4,7 However, various butterflies (Lepidoptera: Lycaenidae, Papilionidae),14,15 weevils (Coleoptera: Curculionidae),7 longhorn beetles (Coleoptera: Cerambycidae),7 bees (Hymenoptera: Apidae),16 jumping spiders (Araneomorphae: Salticidae),17 and tarantulas (Mygalomorphae: Theraphosidae)18 (see Supporting Information Table S1 for a full list of

rganismal colors are commonly produced by pigments that selectively absorb specific wavelengths of light and re-emit others.1 However, many organisms also routinely produce vivid structural colors by constructive interference of light scattered by mesoscale (100−350 nm) biophotonic nanostructures that are diverse in form and optical function.1−4 Arthropods, insects in particular, are the most abundant, diverse, and colorful animals on Earth. Arthropod structural colors function in a variety of contexts including social and sexual signaling, camouflage, and warning or aposematic communication.5−8 A burgeoning number of studies demonstrate that arthropods are an excellent source of biological inspiration for emerging technologies, such as in sensing, and photonics2−4,7,9−13 (also see Supporting Information Table S1 for list of references). © XXXX American Chemical Society

Received: January 18, 2015 Revised: April 30, 2015

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Figure 1. Representative morphology of structural color producing arthropod cuticular nanostructures. (a−f) Light micrographs, (g−l) electron micrographs, and (m−r) representative 2D SAXS patterns from the photonic scales or setae of the following: (a,g,m) Platyaspistes venustus (Curculionidae), single gyroid (I4132) (see Supporting Information Figure S1.105); (b,h,n) Eupholus quintaenia (Curculionidae), single diamond (Fd3̅m) + face-centered orthorhombic (Fddd) (see Supporting Information Figures S1.41 and S1.42); (c,i,o) Sternotomis pulchra (Cerambycidae), simple cubic or single primitive (Pm3̅m) (see Supporting Information Figure S1.130); (d,j,p) Anoplophora graaf i (Cerambycidae), quasi-ordered + fcc opal (see Figure 2d and Supporting Information Figures S1.123 and S1.124); (e,k,q) Amegilla cingulata (Apidae), inverse 2D hexagonal columnar (see Figure 2i and Supporting Information Figure S1.137); and (f,l,r) Thyreus nitidulus (Apidae), inverse 2D twisted columnar (see Figure 2h, and Supporting Information S1.139). False color SAXS patterns (unmasked) depict the logarithm of scattering intensity as a function of the scattering wave vector, q. The radii of the concentric circles are given by the peak scattering wave vector (qpk) times the moduli of the assigned hkl indices of permitted Bragg reflections for the assigned space groups. Crystallographic motifs seen in the SEM images are identified in panels g−i. Panel k and its inset respectively show longitudinal SEM, and cross-sectional TEM views of the setae interior. Scale Bars: a, 25 μm; b−f, 50 μm; g,h, 500 nm; i, 250 nm (inset, 100 nm); j, 100 nm; k, 250 nm (inset, 1 μm), l−600 nm (inset, 500 nm); m−r, 0.05 nm−1. Abbreviations: c, chitin; a, air void.

references) have structurally colored integumentary scales or setae on their wings, elytra, abdomen, and legs. These trichogen-based scales and setae possess a variety of complex, three-dimensional biophotonic nanostructures composed of the polysaccharide chitin, cuticular proteins, and air (reviewed in refs 2−4, 7, and 15). Despite the growing body of research on arthropod structural colors (Supporting Information Table S1), we currently lack accurate structural characterizations of more than a few species. Although knowledge of the development of biophotonic crystals in arthropods is growing,14,19−21 we still lack a comparative developmental framework to understand the rich biodiversity of arthropod cuticular biophotonic nanostructures (discussed in refs 14 and 15) or how these biological signals function and evolve in these organisms. These complex nanostructures are too large to be developing via classical morphogenesis as seen in molecular/cell biology, and much too small to be understood using a multicellular developmental biology framework.14 They are also of broader biomimetic interest, because synthetic fabrication of three-dimensional photonic nanostructures at these rather large optical length scales remains challenging.22−25 Recently, we applied synchrotron small-angle X-ray scattering (SAXS) to identify single gyroid (I4132) photonic crystals in wing scales of five well-studied butterflies from two families14 and single diamond (Fd3̅m) photonic crystals in the cover scales of a fossil weevil Hypera diversipunctata.26 Here, we apply SAXS to structurally characterize the biophotonic nanostructures present within scales and setae from 140 distinctly colored integumentary patches of diverse land arthropod taxa with prominent structural coloration. We supplemented our SAXS assays with electron microscopy (EM) for 44 out of the 140 patches. Our sample includes 129 different color patches from ∼98 species in 75 genera belonging to 9 families of beetles (Coleoptera), single patches from 3 species in 2 genera of bees (Hymenoptera: Apidae: Apinae), single patches from 6 species in 6 genera belonging to 2 families of spiders (Araneae), in

addition to one lycaenid butterfly (Lepidoptera: Lycaenidae) and a bee fly (Diptera: Asiloidea: Bombyliidae) (Supporting Information Table S1).

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RESULTS We find no evidence of a coherently scattering nanostructure present in 19 out of the 140 distinctly colored integumentary patches (Supporting Information Figure S1 and Table S1). The SAXS patterns from the rest of the arthropod scales and setae examined ranged from a large number of discrete Bragg spots in the azimuthal directions (Figure 1m−o,q and Supporting Information Figure S1), characteristic of a polycrystalline nanostructure, to a series of concentric powder-like (or Debye−Scherrer) diffraction rings (Figure 1p,r and Supporting Information Figure S1), characteristic of an amorphous or quasi-ordered nanostructure with only short-range isotropic order.14,27,28 The presence of a large number of sharp, higherorder diffraction spots up to 8 or 9 orders from some weevil and longhorn beetle scales (Figures 1m−o, 2a−c, and Supporting Information Figure S1) underscores a high degree of spatial order for a biological system. However, like SAXS experiments on synthetic soft materials,27 40 of the 121 cases exhibited SAXS spectra with variable or ambiguous features that were intermediate between the idealized predictions of crystalline structures. This could be due to both variation in length scale of peak structural correlations due to finite longrange ordering, which may broaden and flatten diagnostic spectral peaks, or owing to variation in nanostructure between different scales of the same species or even different domains within a single species. For these cases, we present a nanostructural diagnosis based on the predominant SAXS spectra distribution, but we recognize these tentative diagnoses with an * in Table S1 (also see Supporting Information). In the following, we present our SAXS nanostructural diagnoses based on assigning the symmetry that is most consistent with the indexed Bragg peaks in the azimuthal B

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Figure 2. Structural diagnoses of representative SAXS profiles of arthropod cuticular photonic nanostructures. The normalized, azimuthally averaged SAXS profiles were calculated from the respective 2D SAXS patterns and shown on a log−log scale (top to bottom). Curculionidae: (a) Pachyrrhynchus reticulatus, single diamond (Fd3̅m) (see Supporting Information Figure S1.84), (b) Chloropholus nigropunctatus, single gyroid (I4132) (see Supporting Information Figure S1.113). Cerambycidae: (c) Sternotomis mirabilis, simple cubic or single primitive (Pm3m ̅ ) (see Supporting Information Figure S1.132), (d) Anoplophora graaf i, quasi-ordered + fcc opal, (see Figure 1d,j,p and Supporting Information Figures S1.123 and S1.124), (e) A. birmanica, bcc spheres (see Supporting Information Figure S1.119), (f) A. versteegi, quasi-ordered spheres (see Supporting Information Figure S1.122). Apidae: (g) Thyreus pictus, sponge (see Supporting Information Figure S1.138), (h) T. nitidulus, inverse 2D twisted columnar (see Figure 1f,l,r, and Supporting Information Figure S1.139), (i) Amegilla cingulata, inverse 2D hexagonal columnar (see Figure 1e,k,q and Supporting Information Figure S1.137), (j) Porod (q−4) background. The colored vertical lines correspond to the expected Bragg peak positional ratios for various alternative crystallographic space groups, presented together for direct comparison. The numbers above the vertical lines are squares of the moduli of the Miller indices (hkl) for the allowed reflections of specific space-groups. The normalized positional ratios of the scattering peaks are indexed to the predictions of specific crystallographic space groups or symmetries according to IUCr conventions.29

profiles according to IUCr conventions,29 complemented with real-space information from electron microscopy for a third of the assays. The diversity of arthropod cuticular nanostructures is best summarized taxonomically because different lineages have evolved distinct classes of biophotonic nanostructures (Figures 1−3 and Supporting Information Figure S1 and Table S1). Triply periodic, bicontinuous networks were relatively restricted in their distribution. Single gyroid (I4132) networks occurred only in photonic scales of snout weevils (Curculionidae; e.g., Platyaspistes venustus, Figure 1a,g,m) and in wing scales of the Lycaenid butterfly Lycaena kasyapa (Lycaenidae; Supporting Information Figure S1.1); However, single gyroid

photonic crystals are so far known in the wing scales of only four other genera within lycaenid and papilionid butterflies.14,15,30,31 Single diamond (Fd3̅m) and sheared, facecentered orthorhombic (Fddd32,33) networks were also found only in snout weevils (e.g., Eupholus quintaenia; Figure 1b,h,n and Supporting Information Figure S1.42). In Lamprocyphus weevils (Supporting Information Figures S1.72−80 and Table S1) for instance, both single diamond and single gyroid photonic crystals were identified on the same individual and sometimes within different domains in the same scale. Spongelike or quasi-ordered versions of single diamond networks with varying degrees of disorder were also present C

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Figure 3. A biophysical framework for classifying the diversity of arthropod cuticular photonic nanostructures. (a) A schematic of the lyotropic phase behavior depicting the well-known equilibrium inverse lipid phases in order of increasingly positive Gaussian curvature (see ref 51), starting with the flat lamellar phase (Lα), whose interfacial mean and Gaussian curvature is trivially zero. These include the inverse bicontinuous cubic phases (QII: double gyroid Ia3̅d, double diamond Pn3̅m, and double primitive Im3̅m), perforated lamellae (L3), inverse hexagonal columnar cylinders (HII) as well as inverse micelles or vesicles that can be jammed or close-packed into cubic (III) or amorphous (L2) arrays. (b) Topological decomposition of lyotropic phases in (a) into constant mean curvature surfaces: plane, saddle (Schoen’s gyroid G, Schwarz’s diamond D, and Schwarz’s primitive P), lamellar-helicoid (Riemann’s minimal surface shown; image credit: Matthias Weber), cylinder, and sphere, along with the corresponding interfacial mean (H) and Gaussian or saddle-splay curvature (KG). Note the first three are minimal surfaces. (c) The diversity and taxonomic distribution of arthropod cuticular photonic nanostructures.

nanostructure of the longhorn beetle Prosopocera lactator was diagnosed as a bcc (Im3̅m) network of connected spheres (cf ref 34). Interestingly, these appear to be structurally intermediate between the close-packed sphere nanostructures of other longhorn beetles and bicontinuous network nanostructures of Sternotomine longhorns. Quasi-ordered arrays of chitin spheres were also identified within scales of two basal taxa of beetles, Toxonotus sp. (Coleoptera: Curculionoidea: Anthribidae) and Isacantha sp. (Coleoptera: Curculionoidea: Belidae). A two-dimensional, inverse hexagonal columnar morphology (i.e., air pores in chitin) was diagnosed in the iridescent setae of a digger bee, Amegilla cingulata (Hymenoptera: Apidae: Anthophorini, Figures 1e,k,q and 2i)16 and in a jumping spider (Araneae: Salticidae, Supporting Information Figure S1.141). A 2D, Bouligand-like,35 twisted inverse columnar morphology was identified in setae of a cuckoo bee, Thyreus nitidulus (Hymenoptera: Apidae: Melectini, Figures 1e,k,q and 2i, and

in weevils, sometimes also within the same individual (e.g., Eupholus bennetti; Supporting Information Figures S1.39 and S1.40 and Table S1). By contrast, the photonic scales of longhorn beetles (Coleoptera: Cerambycidae) possessed nanostructures essentially based on ball-and-stick arrangements of chitin spheres. One class of nanostructure found in the photonic scales of longhorn beetles consisted of ordered (face-centered cubic, fcc; body-centered cubic, bcc) and quasi-ordered close-packing of discrete chitin spheres sometimes connected by thin necks (Coleoptera: Cerambycidae; e.g., Anoplophora graaf i; Figures 1d,j,p and 2d and Supporting Information Figures S1.123− 124). Single primitive or simple cubic (Pm3̅m) triply periodic bicontinuous networks as well as quasi-ordered or sponge-like versions of the same were present only in the Sternotomini tribe of longhorn beetles (Coleoptera: Cerambycidae; e.g., Sternotomis pulchra bifasciata, Figure 1c,i,o and Supporting Information Figures S1.130−131). The scale photonic D

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Nano Letters Supporting Information Figure S1.139), and in scales of Hoplia scarab beetles (Coleoptera: Scarabaeidae, Supporting Information Figures S1.3−4).36 Amorphous or quasi-ordered, spongelike networks were diagnosed in the photonic setae of another species of the same genus of cuckoo bee, T. pictus (Supporting Information Figure S1.138). Lastly, the photonic nanostructures in purple-blue setae of tarantulas (Araneae: Theraphosidae, Supporting Information Figures S1.142−145) were characterized as perforated lamellae, as in many butterflies.15,18,20,37,38 The SAXS structural data also confirm that the arthropod cuticular nanostructures are sufficiently ordered at the appropriate length scales to produce the observed colors via constructive interference (Supporting Information Figure S2). We have thus assayed the cuticular scale and setae nanostructure of ∼127 species of land arthropods in 85 genera belonging to 4 orders of insects and two suborders of spiders using SAXS and EM, including ∼66 genera that have not to our knowledge been previously investigated. The analysis has resolved uncertainties in the diagnoses of the biophotonic nanostructure in previous studies (Supporting Information Table S1). Compared to birds,28,39,40 lizards and frogs,41 cephalopods and other aquatic animals,13,42 terrestrial arthropods, especially insects, exhibit a breath-taking array of biophotonic nanostructures within scales and setae. Intriguingly, the diversity of arthropod photonic nanostructures documented here exhibits the very same, rich polymorphism found in amphiphilic macromolecules, such as block copolymers,43−46 surfactants,47 and lipids.48,49 Biological lipid bilayer membranes are known to self-assemble in aqueous media into a variety of inverse or type-II lyotropic liquid crystalline phases or morphologies50,51 (Figure 3a). In addition to their crystallographic space group symmetries, these selfassembled membrane phases can be classified based on the variation in their interfacial curvature.48,50−52 The fundamental geometry of these lyotropic phases can then be topologically classified into sphere, cylinder, or the associate (Bonnet) families of lamellar-helicoid (Riemann’s) and saddle (Schwarz’s D, P, and Schoen’s G) surfaces. All of these surfaces are characterized by a constant mean curvature (H = (c1 + c2)/2) but they can be differentiated on the basis of their Gaussian or saddle-splay curvature (KG = c1c2, where c1 and c2 are the principal curvatures along orthogonal planes perpendicular to the surface)53,54 (Figure 3b). The Gaussian curvature of a sphere is positive, zero for cylinders and planes, and negative for a saddle. Furthermore, lamellar, lamellar-helicoid, and saddle morphologies are examples of minimal surfaces, that is, they have zero mean curvature. Even in a quasi-ordered sponge or a perforated lamellar morphology, the pores may be thought of as a Riemann’s minimal surface with helicoid-like bridges connecting adjacent, asymptotic, and parallel (lamellar) planes55−57 (Figure 3b). The similarity of arthropod cuticular nanostructures to amphiphilic block copolymer, surfactant, and lyotropic lipid phase states is not merely a structural or geometrical analogy. Biological lyotropic lipid membrane morphologies, including the triply periodic, bicontinuous cubic phases (double gyroid, double diamond, and double primitive morphologies) are wellknown in membrane-bound organelles of living cells.57−66 However, these arthropod biophotonic nanostructures are much larger in size (lattice parameters of 50−500 nm)50,61,65 than those produced by typical lipid−water systems (≤20 nm).51

The self-assembly of biological lipid bilayer membranes into lyotropic morphologies is hypothesized to be regulated by the energetics of membrane curvature.50,63,67 Living cells control the curvature and shape of their membranes with membranebinding proteins that vary in shape, molecular weight, and electrostatic properties.52,63−65,67,68 We hypothesize that multiple lineages of arthropods have independently evolved to utilize the intrinsic capacity of membrane-bound organelles to selfassemble into lyotropic phases to template the precursors of color producing nanostructures. Specifically, we posit that the controlled expression of membrane-binding proteins with different bilayer bending (κ) and Gaussian or saddle-splay (κ)̅ moduli51,52 in arthropod scales and setae cells could similarly facilitate the development of various lyotropic precursor templates of biophotonic nanostructures.50,61,65,66,68 It is also likely that the curvature of these biological nanostructures are stabilized by intermembrane binding proteins.68 Interestingly, each arthropod lineage studied has evolved to occupy different portions of the total lyotropic phase space (Figure 3c). For instance, many different arthropod families exhibit quasi-ordered sponge-like networks or perforated lamellae. But single gyroid and single diamond nanostructures are found only in curculionid weevils, and lycaenid and papilionid butterflies. Likewise, quasi-ordered and ordered close-packings of chitin spheres are found only in longhorn beetles and in two basal families of weevils. Thus, it appears likely that within each lineage the molecular structure of the membrane-binding proteins has evolved to express only a limited range of the total possible physical effects on membrane curvature and stability.50−52 The plausibility of this model is supported by the existence of the highly conserved superfamily of BAR-domain proteins, which have been shown to affect and stabilize membrane curvature in endocytic spherical or tubular invaginations,67,69 for example, in three-dimensional, cubic membrane (t-tubule) networks in striated skeletal muscle cells.58,70 This model suggests a likely biophysical framework for understanding the developmental basis and biodiversity of arthropod photonic nanostructures (Figure 3). The distinctly nonrandom distribution of the cuticular biophotonic nanostructures in arthropods also implies apomorphic (lineagespecific) differences in membrane-folding mechanisms (see below). In butterflies, the single gyroid photonic crystals in wing scale cells have been hypothesized to develop from a core−shell double gyroid (Ia3̅d) template made by tandem infolding of the smooth endoplasmic reticulum (SER) and plasma membranes,14,19−21 as in core−shell morphologies seen in triblock copolymer systems.71,72 After development of the core−shell double gyroid template, chitin is deposited into the extracellular space, which is continuous with one of the two single gyroid cores. Upon maturation, the rest of the scale cell dries up and dies, leaving behind a single gyroid (I4132) network comprising chitin and air of the appropriate size to constructively reflect a specific visible color.14 Double gyroids can be directly selfassembled, unlike single gyroids (which have superior optical properties73). Therefore, butterflies have evolved to selfassemble a double gyroid template from the interactions of plasma and SER membranes, but use only one of the two single gyroid compartments to bioengineer the final optical nanostructure.14 The development of biophotonic nanostructure within scale cells has been investigated only in a few butterflies.19−21,74 Nevertheless, given the homology of the trichogen (shaftE

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Nano Letters forming cells) across all arthropods,75 the development of photonic nanostructures in scales and setae of other insects and spiders likely proceeds via similar membrane-folding mechanisms. However, the diversity of optical nanostructures observed in arthropod integument requires recognition of two broad classes of biophysical developmental mechanisms. The first class can lead to self-assembly starting from a single lipid bilayer interface dividing two aqueous volumes.44,45,51 These nanostructures include spongelike quasi-ordered networks, perforated lamellae, inverse (hexagonal and twisted) columnar phases, and quasi-ordered and ordered (fcc, bcc) sphere packings. These morphologies likely develop within scale cells from the infolding of the plasma membrane into a lyotropic template, followed by extracellular chitin deposition and the maturation of the cell. By contrast, the second class leads to the self-assembly of single gyroid and single diamond nanostructures of snout weevils from double gyroid or double diamond precursor templates. This process requires the collaborative infolding of both the plasma membrane and SER, as observed in lycaenid butterflies.14,21 These developmental hypotheses are further supported by the observation that single gyroid and single diamond networks in butterfly14 and weevil scales have relatively low chitin filling fractions (mean 0.2; Supporting Information Table S1). The low volume of chitin results from the fact that the final cuticular nanostructure consists of only one of a pair of chiral interpenetrating networks. The similarity of weevil scale development to that of butterflies is further supported by the presence of one or more submicron vesicles in weevil scales (e.g., see Supporting Information Figure S1.44) that appear to be vestiges of SER fragments hypothesized to play a role in organizing the parallel membranes.21 On the other hand, the biophotonic nanostructures in longhorn beetles and bees have significantly higher (unpaired t = 7.6, df = 41, P < 0.0001) chitin filling fractions (mean 0.48; Supporting Information Table S1). Therefore, unlike butterflies or weevils, these larger chitin volume fractions eliminate the physical space for the parallel infolding of a second lipid bilayer within the developing scale cells. Interestingly, like other longhorn beetles, the single primitive or simple cubic triply periodic bicontinuous networks of Sternotomis longhorn beetles also have high chitin filling fractions (0.4, on average; Supporting Information Table S1), which would prevent the infolding of a second parallel bilayer membrane during their development. So, they appear to share a common developmental mechanism with other longhorn beetles. This underscores the phylogenetic constraints on the development and evolution of biophotonic nanostructures. We illustrate these possible developmental scenarios by analogy to the microphase separation of block copolymers (Figure 4). As in butterflies,14 we posit that single gyroid and single diamond nanostructures in snout weevil scales develop via the tandem infolding of parallel plasma and SER bilayer membranes, akin to a linear ABC triblock copolymer that is compositionally asymmetrical about the midplane, that is, ABCB′A′ (Figure 4a).76 A core−shell double gyroid (Ia3d̅ ) or a double diamond (Pn3̅m) precursor thus self-assembled is transformed into a single gyroid or single diamond by backfilling only one of the core volumes (which is continuous with the extra-cellular space) with chitin. By contrast, we propose that scale or setae nanostructures in longhorn beetles, bees, and spiders develop only by the invagination of the plasma membrane, similar to an AB diblock copolymer that is compositionally asymmetrical about the midplane, that is, ABA′

Figure 4. Self-assembly of arthropod cuticular photonic nanostructures, by analogy to microphase separation in block copolymers. (a) As in butterflies,14 single gyroid (I4132) (illustrated) and single diamond (Fd3m ̅ ) scale nanostructures in snout weevils likely develop via tandem infolding of parallel plasma and SER bilayer membranes into a precursor, core−shell double gyroid (Ia3d̅ ) (illustrated) or double diamond (Pn3̅m) template within the perimeter of the scale cell. This is akin to a linear ABC triblock copolymer, which is compositionally asymmetrical about the midplane (ABCB′A′). (b) Scale and setae nanostructures in longhorn beetles, bees, and spiders likely develop by the invagination of the plasma membrane only, similar to an AB diblock copolymer that is compositionally asymmetrical about the midplane (ABA′/ABC) to produce nanostructures with the observed ∼50% volume fractions (as illustrated for the Pm3m ̅ nanostructure). In both panels a and b, the extracellularly synthesized biopolymer chitin is deposited into only one of the interpenetrating volumes (A), which is continuous with extracellular space, and the subsequent desiccation and degeneration of the rest of the dying cell results in the final photonic nanostructure (middle and right columns). The biological components of the developing scale or setae cell are shown colorcoded to the different monomer blocks of a hypothetical linear noncentrosymmetric ABCB′A′ or ABA′/ABC block copolymer (leftmost column).

or ABC (Figure 4b) to produce nanostructures closer to 50% volume fractions. In both cases, chitin, which is an extracellular polymer, is then deposited into the extracellular space (A), and the subsequent desiccation and degeneration of the rest of the dying cell results in the final photonic nanostructure. Future observations and experiments on the development of scale and setae nanostructures in weevils, longhorn beetles, and other arthropods are necessary to test these hypotheses. Cellular control of the physical mechanisms of lipid bilayer self-assembly has likely enabled many arthropod lineages to evolutionarily explore most of the phase space of lyotropic or amphiphilic materials for a photonic function at optical length scales not easily achieved in synthetic soft matter systems.45,51 The repeated evolutionary co-option of the biological membrane self-assembly provides a novel, generalized explanation for the explosive diversity of photonic nanostructures in arthropod scale and setae cells. Future experiments should focus on identifying putative proteins that control membrane curvature and invagination within scale or setae cells during development. These diverse arthropod biophotonic scales may offer convenient biotemplates to serve in functional applications F

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Nano Letters such as sensing10 and photonics77 (after appropriate dielectric infiltration). At the same time, protein-mediated membrane self-assembly of synthetic bilayer membranes,68 and the phase behavior of a linear, noncentrosymmetric pentablock copolymer obtained by the mixing of a ternary triblock and a binary diblock copolymer with suitably optimized molecular weights to maximize the lattice parameters76 are two perhaps promising bioinspired (if not biomimetic) approaches to synthesizing tunable mesophases with large lattice parameters, including morphologies like single gyroid and single diamond currently not accessible via direct synthetic self-assembly.24

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Hope Entomological Collections (James Hogan, Ray Gabriel, and Darren Mann), Smithsonian U.S. National Museum Entomology Collections (Steve Lingafelter), and CSIRO Australian National Arthropod Collection (ANIC). We thank Nick Terrill and Tobias Richter for help with SAXS data collection at beamline I22 of the Diamond Light Source that contributed to some of the results presented here, as well as Stephen Mudie, Sarah Weisman, and Tara Sutherland for comments and support regarding specimen preparation for SAXS at the Australian Synchrotron.

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ASSOCIATED CONTENT

S Supporting Information *

Detailed SAXS structural diagnoses, SAXS optical reflectance predictions, and coherence length estimates of arthropod cuticular photonic nanostructures, and materials and methods. The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.nanolett.5b00201.

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REFERENCES

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. Present Addresses

(V.S.) Life Sciences, Yale-NUS College, 6 College Avenue East, 138614, Singapore (A.E.S.) Agricultural Scientific Collections Unit, NSW Department of Primary Industries, Orange Agricultural Institute, 1447 Forest Road, Orange NSW 2800, Australia Author Contributions

V.S., A.E.S., A.S., S.N., and R.O.P. designed the research; V.S. and A.E.S. performed research; all authors discussed and/or analyzed the data; V.S. and R.O.P wrote the manuscript with inputs from S.G.J.M, E.R.D., and C.O.O. Funding

SAXS data collection at 8-ID, Advanced Photon Source, Argonne National Laboratory, was supported by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences, under Contract DE-AC02−06CH11357. This work was supported with seed funding from the US National Science Foundation (NSF) Materials Research Science and Engineering Center (DMR 1119826) and NSF grants to S.G.J.M. (DMR0906697), H. C. (PHY-0957680), a Royal Society Newton Fellowship and Linacre College EPA Junior Research Fellowship to V.S. as well as Yale University W. R. Coe Funds to R.O.P. R.O.P. acknowledges the support of the Ikerbasque Science Fellowship and the Donostia International Physics Center. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank Bill Krinsky, Steve Lingafelter, Rick Leschen, and Rolf Oberprieler for assistance with arthropod identification, Pietro De Camilli for stimulating discussions on protein− membrane interactions, Antonia Monteiro, and two anonymous reviewers for helpful comments on this manuscript. Arthropod specimens were kindly provided by the Yale Peabody Museum of Natural History Entomology Collections (Larry Gall), University of Oxford Natural History Museum G

DOI: 10.1021/acs.nanolett.5b00201 Nano Lett. XXXX, XXX, XXX−XXX

Letter

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