Evolutionary Photonics: Structure, function, development and evolution of organismal structural color

Structural colors are prominent in nature and constitute an important aspect of the organismal phenotype, and are frequently used in social and intersexual communication. The underlying color-producing or biophotonic nanostructures are diverse in form and function. Their structural and optical characterization have remained challenging despite a century of research. Prior to this dissertation, biophotonic nanostructures have only been examined with various electron microscopy (EM) and tomography techniques in a relatively small number of species. This dissertation has developed the use of synchrotron Small Angle X-ray Scattering (SAXS) as a precise, high-throughput tool for diagnosing biophotonic nanostructures, as well as predicting their single scattering optical function and represents a substantial improvement over previous techniques.;In birds, the nanostructure and optical properties of 255 non-iridescent, structurally colored feathers from 194 diverse species in 41 families, encompassing the gamut of non-iridescent structural hues, were assayed using SAXS. This enabled a precise quantitative, comparative diagnosis and characterization of the 3D amorphous or quasi-ordered barb photonic nanostructures. By examining a wide range of species across Aves, the structural data from the two classes of barb nanostructures were found to be strikingly similar to those of self-assembled morphologies seen during the phase separation of synthetic polymers via spinodal decomposition and nucleation-and-growth. These results support the hypothesis that multiple independent lineages of birds have independently evolved quasi-ordered feather nanostructures that are self-assembled by the phase separation of polymerizing beta-keratin from the cytoplasm of medullary cells.;The complex photonic crystal nanostructures found in the iridescent, structurally colored scales of some butterflies, broad-nosed weevils, flat-nosed long-horned beetles and a few bees were also diagnosed using SAXS. A broad diversity of chitin and air nanostructures within photonic insect scales was identified including: bicontinuous cubic networks---single gyroid, single diamond, and simple cubic; amorphous and ordered close-packings of spheres; inverse 2D hexagonal lattice; and a disordered sponge morphology. Accurate structural knowledge of the insect scale photonic nanostructures led to the realization that the biological soft matter systems responsible for the complex insect photonic nanostructures characterized here have evolutionarily explored most of the phase space or parameter space documented in soft condensed matter physics. Given the homology of insect scale cells, insects have apparently evolved their diversity of scale nanostructures by manipulating membrane-folding energetics mediated by the binding of curvature-inducing proteins to arrive at different evolutionarily stable self-assembled phase states.;The self-assembled, amorphous photonic nanostructures in bird feather barbs with a pronounced isotropic short-range order and the diversity of lyotropically self-assembled insect scale nanostructures could therefore offer a useful biotemplate for the design and manufacture of a variety of optically-tunable, self-assembled mesophases for photonic applications, based on biomimicry or direct dielectric infiltration.;The application of SAXS to organisms' nanostructures has revealed fascinating insights into the development of biophotonic nanostructures. The self-assembly hypothesis for the development of photonic nanostructures in birds and insects offers an coherent and elegant explanation for the repeated independent evolution of distinctive and highly stereotyped versions of a variety of biophotonic nanostructures in ecologically and evolutionarily diverse lineages.