Physics, Development, and Evolution of Structural Coloration

Unlike the colors produced by molecular pigments, the structural colors of organisms are produced by the physical interactions of light with nanometer scale biological structures. I became interested in structural colors through my studies of the evolution of intersexual display behavior and communication (See Phylogenetic Ethology and Sexual Selection link). In our first examination of structurally colored bird skin, we stumbled upon a previously undescribed mechanism of structurally coloration in skin- coherent scattering, or constructive interference, from parallel collagen fibers (Prum et al. 1994 link). In subsequent research, I teamed up with mathematician Dr. Rodolfo Torres of the University of Kansas Department of Mathematics to develop a new application of Fourier analysis to investigate structural color production by biological nanostructures.

Our first contribution to the physics of structural coloration has been the identification of a class of “quasi-ordered” or “amorphous” biological nanostructures– which are ordered only at the local scale– that produce non-iridescent structural colors by the mechanism of constructive interference, or coherent scattering. Coherent scattering is the selective reinforcement of a particular portion of the light spectrum because of nanoscale spatial periodicity in variation in refractive index. Many well known biological structural colors are produced by laminar or crystal-like arrays of materials of different refractive indices. Laminar or crystal-like arrays typically produce iridescence, or a prominent change in color with angle of observation and illumination. In contrast, quasi-ordered nanostructures are sufficiently ordered at the spatial scale of nearest neighbors, but they lack the higher level order of the laminar and crystal-like arrays. As a consequence, the average differences in path length additions among light waves back scattered by a quasi-ordered array are the same for many different angles. This nanostructure creates coherent scattering of a select range of wavelengths without creating the conditions for iridescence. Because of their lack of iridescence, many color producing quasi-ordered arrays have been erroneously hypothesized to produce color by incoherent scattering (or Rayleigh, Tyndall, or Mie scattering). By examining the spatial periodicity of variations in refractive index, we can test whether these biological nanostructures produced colors by coherent or incoherent scattering.

We have documented structural color producing by quasi-ordered arrays in the spongy medullary layer of bird feathers in dermal collagen arrays of bird skin, and in evolutionarily convergent arrays in mammal skin. Because we have falsified so many hypothesized examples of incoherent scattering in organisms, we are also testing alternative hypotheses of color production in blue dragonflies (Odonata), structurally colored butterflies (Lepidoptera), and the human iris.

Little research has been done on the evolution and development of color producing nanostructures. The origin of structural color production requires the evolution of periodic optical nanostructures from some plesiomorphic organization. We have also identified instances of the evolutionary transitions between quasi-ordered and crystal-like nanostructures. The Fourier Tool provides a new, alternative method for the comparative, optical analysis of diverse nanostructures, and can provide the first method for optical analysis of transitions among major classes of coherently scattering nanostructures.

Future work is focusing on the evolution of color producing nanostructures within avian clades, the development of self-assembled optical nanostructures, and mathematical simulations of the evolution of nanostructure in response to optical selection (i.e. sexual or social selection on structural color).

References

Prum, R. O., Morrison, R. L., and Ten Eyck, G. R. 1994. Structural color production by constructive reflection from ordered collagen arrays in a bird (Philepitta castanea: Eurylaimidae). Journal of Morphology 222: 61-72.

Prum, R. O., Torres, R. H., Williamson, S., and Dyck, J. 1998. Coherent light scattering by blue bird feather barbs. Nature 396: 28-29.

Prum, R. O., Torres, R. H., Williamson, S., and Dyck, J. 1999. Two-dimensional Fourier analysis of the spongy medullary keratin of structurally coloured feather barbs. Proceedings of the Royal Society, London: Biological Sciences (B) 266: 13-22.

Prum, R. O. 1999. The anatomy and physics of avian structural colours. In: Proceedings of the XXIInd International Ornithological Congress. Adams, N. J. and Slotow, R. H. (eds.). S29.1: 1633-1653. Johannesburg: BirdLife South Africa.

Prum, R. O., Andersson, and S. F., Torres, R. M. 2003. Coherent scattering of ultraviolet light by avian feather barbs. Auk 120:163-170.

Prum, R. O., and Torres, R. H. 2003. Structural colouration of avian skin: Convergent evolution of coherently scattering dermal collagen arrays. Journal of Experimental Biology. 206: 2409-2429.

Prum, R. O., and Torres, R. H. 2003. A Fourier tool for the analysis of coherent light scattering by bio-optical nanostructures. Integrative and Comparative Biology 43: 591-610.

Prum, R. O., and Torres, R. H. 2004. Structural colouration of mammalian skin: Convergent evolution of coherently scattering dermal collagen arrays. Journal of Experimental Biology. In press.

Prum, R. O., and Torres, R. H. 2004. Structural colouration of mammalian skin: Convergent evolution of coherently scattering dermal collagen arrays. Journal of Experimental Biology 207: 2157-2172.

Prum, R. O., Cole, J. A., and Torres, R. H. 2004. Blue integumentary structural colours in dragonflies (Odonata) are not produced by incoherent Tyndall scattering. Journal of Experimental Biology 207:3999-4009.

Prum, R. O., Quinn, T., and Torres, R. H. 2006. Anatomically diverse butterfly scales all produce structural colours by coherent scattering. Journal of Experimental Biology 209: 748-765.

Shawkey, M. D, , Saranathan, V., Pálsdóttir, H., Crum, J., Ellisman, M., Auer, M., Prum, R. O. 2009. Electron tomography, three-dimensional Fourier analysis and colour prediction of a three-dimensional amorphous biophotontic nanostructure. Journal of the Royal Society Interface doi:10.1098/rsif.2008.0374.focus

Prum, R. O., E. R. Dufresne, Quinn, T., and Waters, K. 2009. Development of colour producing b-keratin nanostructures in avian feather barbs. Journal of the Royal Society Interface In Press.

Prum, R. O., Dufresne, E. R., Quinn, T., and Waters, K. 2009. Development of colour producing ?-keratin nanostructures in avian feather barbs. Journal of the Royal Society Interface 6:S253-S265. doi:10.1098/rsif.2008.0466.focus

Dufresne, E. R., Noh, H., Saranathan, V., Mochrie, S., Cao, H., and Prum. R.O. 2009. Self-assembly of biophotonic nanostructures by phase separation. Soft Matter 5:1792-1795. doi:10.1039/b902775k.