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78.1 - Fall 2004

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By Michael Nkansah

Animals put their many colors to an eclectic variety of uses. While birds like the peacock lusciously display their colorful plumage during courtship, amphibians like the poison dart frog release brightly colored, poisonous secretions for defense against predators. The milk snake, mountain king snake, and Colorado desert sand snake of the western United States have colorful banding patterns, which closely resemble that of the much more poisonous Arizona coral snake, enabling them to ward off potential predators.

Most of the colors that animals display are produced from pigments. In humans, skin color variation is caused primarily by differences in size and distribution of the pigment melanin. Birds, on the other hand, use carotenoid pigments in their feathers to produce the bright red and yellow colors they are noted for.

The lurid glow of a mandrill’s face tells yet another of nature’s colorful stories. For years, blue-colored mammals have attracted much scientific interest, study, and speculation. Vertebrates, in general, have not been evolutionarily endowed with the capacity for producing blue pigment internally. Most vertebrates cannot even see the color, which explains why the evolution of blue pigments in vertebrates has been generally retarded. This consequently suggests that primates like the West African mandrill and vervet monkey, as well as marsupials like the mouse opossum, must be producing their blues in some other way.

In living systems, the most common source of coloration is pigmentation, in which portions of an incident light spectrum are absorbed while the remaining wavelengths are reflected as the color we perceive. The utter absence of blue pigments in mammals, however, has driven scientists over the past century to search for more structural explanations like the one given for the color of the sky.

The blue of the sky results from incoherent scattering of light particles rather than from pigmentation. In this mechanism, also known as Rayleigh/Tyndall scattering, the random, small-sized structures of nitrogen and oxygen present in the atmosphere preferentially scatter the small wavelengths of light — blue and violet — allowing longer ones to pass through. The resulting color we see is the scattering of blue and violet light. Until now, scientists have used this same explanation for mammalian blue.

Professor Richard Prum’s work has provided important cues to our understanding of how coloration evolved in mammals. (Credit: Mike Marsland)

According to Richard Prum, professor of ecology and evolutionary biology and curator of vertebrate zoology at the Peabody Museum, scientists to date may very well have been wrong about the actual details of how the coloration occurs. Working in collaboration with a University of Kansas mathematics professor, Rodolfo Torres, Prum has shown that mammalian blue results more from coherent scattering of light rather than incoherent scattering.

Coherent scattering is what gives opal gems and oil slicks their iridescent color. Opal gems have crystal planes, and oil slicks have laminar layers, the parallel layers formed in non-turbulent streamline flow. These regularly arranged structures allow oil slicks and opal to scatter light at different angles, producing different hues of color. Whereas incoherent scattering models require the reflecting surfaces to be at randomized positions relative to the incident light, coherent scattering models require reflecting surfaces to have non-random, highly regular organization relative to incident light. Hence color produced from coherent scattering is described in terms of the phase interactions between light reflected from multiple surfaces. Incoherent scattering, however, considers each reflecting surface as spatially independent from the others and describes color as a function of the light reflected from individual surfaces.

Scientists had adopted the earlier explanation as an easy generalization from what was seen in the case of the sky, one where a non-iridescent color is produced by incoherent scattering. But they were wrong. The mistake was due in part to a sloppy characterization of all non-iridescent colors as incoherently produced, Prum explains. Mammalogists had assumed that melanocytes, biological colloids, or turbid protein media present in the dermis served as the randomized reflecting surfaces required by Tyndall scattering when, in reality, the dermal collagen fibers were responsible for producing the color.

Transmission electron micrographs of collagen arrays from structurally colored mammal skin. (A) Female mandrill facial skin. Scale bar, 500 nm. (B) Male mandrill rump skin. Scale bar, 1000 nm. (C) Male mandrill facial skin. Scale bar, 250 nm. (D) Male mandrill rump skin. Scale bar, 250 nm. (E) Vervet monkey scrotum. Scale bar, 500 nm. (F) Mouse opossum. Scale bar, 100 nm. (Credit: Journal of Experimental Biology)

The erroneous assumptions of previous scientists could certainly be understood in light of the fact that cutting-edge technology needed for high-resolution nanostructural analysis became available only recently. So when Prum stumbled sometime last year across a museum-preserved Madagascan bird, the velvet asity, whose once green wartle had turned blue, he put his scientific hunch to the test. By studying the layers of collagen fiber present in the skin using electron microscopy, he observed hexagonally organized crystal-like arrays of parallel collagen fibers in the dermis — a level of organization that defied all conditions necessary for Rayleigh scattering. The surfaces observed were neither random nor spatially independent.

Working with Torres in Kansas, the two used a newly developed application of Discrete Fourier Transform (DFT). The Fourier tool decomposes an image into different periodic components, transforming discrete data into a combination of sine waves with different amplitudes and frequencies. The relative squared amplitudes of these component waves, called a Fourier power spectrum, then express the contribution of each variation’s frequency to the original data by indicating which frequency carries the most energy. The tool’s operation relies heavily on the use of a Fast Fourier Transform (FFT), which is a computer algorithm used in computing the DFT.

Following on the electromagnetic theory of corneal transparency by George Benedek of Massachusetts Institute of Technology, Prum and Torres used the 2D Fourier power spectrum of transmission electron micrographs of biological nanostructures in characterizing the spatial periodicity in refractive index variation within these structures. According to Benedek’s theory, any such periodicity would result in the reinforcement of a limited set of wavelengths. Hence the tool was used to test whether spatial variation in refractive index was random, as required for incoherent scattering, or periodic, as required for coherent scattering.

The bird’s blue wattle, it turned out, had a nanostructural organization that was not only comparable with those found in crystal lattices but also capable of scattering light particles coherently. Treatment with ethanol preservative had shrunk the dermal tissue, bringing fibers closer to one another and changing the wavelength they reflected. A subsequent study of a sister avian family, the sunbird asities, revealed less regular coherently scattering nanostructures, which Prum and Torres describes as “quasi-ordered.”

Prum’s observations provided the first phylogenetically documented instance of macroevolution between classes of coherently scattering nanostructures. For such periodic arrays, the 2D Fourier power spectrum could distinguish between laminar, crystal-like, and quasi-ordered nanostructures since laminar and crystal-like typically produce iridescence while quasi-ordered arrays do not.

Using the Fourier tool, Prum was able to correctly classify the structural color of several avian species like Philepitta castanea, which were previously believed to produce color by incoherent scattering. This began his year-long odyssey of identifying similar structures in mammals.

Studying the blue skin of mammals in similar fashion, Prum also observed quasi-order within the collagen fibers in the dermal medullary layer of the skin. In the June 15, 2004 issue of the Journal of Experimental Biology, Prum and Torres discussed the results of their ground-breaking research, suggesting that quasi-ordered nanostructure may have evolved convergently in the skins of mammals and birds. Prum’s seminal work in investigating biological nanostructures adds yet another entry to our long list of complex mechanisms nature employs in reaching its elusive ends.

MICHAEL NKANSAH is a sophomore in Calhoun College majoring in chemical engineering.

The author appreciates Professor Richard O. Prum’s help in preparing this article.

Science Links

Present your research to New Haven high school students (Synergy Outreach) Astronomy Picture of the Day (NASA) BBC Science & Nature (BBC) Learn how our lifestyles can change the way our genes work, examine a yet-to-be-broken code on a sculpture called Kryptos, see preserved dinosaur blood vessels (NOVA ScienceNow) Watch Health Videos: Weight-loss surgery to caffeine on the brain (CNN Health News) Science, Health, Environment & Technology (ScienceDaily)

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