Patterns And Processes Of Diversification: Speciation And Historical Congruence In Some Neotropical Birds

Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/137456/1/evo04164.pd

Structural colouration of avian skin: convergent evolution of coherently scattering dermal collagen arrays

Structural colours of avian skin have long been hypothesized to be produced by incoherent (Rayleigh/Tyndall) scattering. We investigated the colour, anatomy, nanostructure and biophysics of structurally coloured skin, ramphotheca and podotheca from 31 species of birds from 17 families in 10 orders from across Aves. Integumentary structural colours of birds include ultraviolet, dark blue, light blue, green and yellow hues. The discrete peaks in reflectance spectra do not conform to the inverse fourth power relationship predicted by Rayleigh scattering. The dermis of structurally coloured skin consists of a thick (100-500 mum) layer of collagen that is usually underlain by a layer of melanin granules. Transmission electron micrographs (TEMs) of this colour-producing dermal collagen layer revealed quasi-ordered arrays of parallel collagen fibres. Two-dimensional (2-D) Fourier analysis of TEMs of the collagen arrays revealed a ring of peak spatial frequencies in the spatial variation in refractive index that are the appropriate size to make the observed ultraviolet-yellow colours by coherent scattering alone. One species, Philepitta castanea (Eurylaimidae), has exceptionally ordered, hexagonal arrays of collagen fibres that produce a hexagonal pattern of spatial frequency peaks in the power spectra. Ultraviolet, blue, green and yellow structural colours of avian skin are produced by coherent scattering (i.e. constructive interference) by arrays of collagen fibres in the dermis. Some yellow and orange skin colours are produced with a combination of structural and pigmentary mechanisms. These combined colours can have reflectance spectra with discrete peaks that are more saturated than hues produced by carotenoid pigments alone. Bluish facial skin from two species of Neotropical antbirds (Thamnophilidae) are nanostructurally too small to produce visible light by coherent scattering, and the colour production mechanism in these species remains unknown. Based on the phylogenetic distribution of structurally coloured skin in Aves, this mechanism of colour production has evolved convergently more than 50 independent times within extant birds

Structural colouration of mammalian skin: convergent evolution of coherently scattering dermal collagen arrays

For more than a century, the blue structural colours of mammalian skin have been hypothesized to be produced by incoherent, Rayleigh or Tyndall scattering. We investigated the colour, anatomy, nanostructure and biophysics of structurally coloured skin from two species of primates - mandrill (Mandrillus sphinx) and vervet monkey (Cercopithecus aethiops) - and two species of marsupials - mouse opossum (Marmosa mexicana) and wooly opossum (Caluromys derbianus). We used two-dimensional (2-D) Fourier analysis of transmission electron micrographs (TEMs) of the collagen arrays in the primate tissues to test whether these structural colours are produced by incoherent or coherent scattering (i.e. constructive interference). The structural colours in Mandrillus rump and facial skin and Cercopithecus scrotum are produced by coherent scattering by quasi-ordered arrays of parallel dermal collagen fibres. The 2-D Fourier power spectra of the collagen arrays from Mandrillus and Cercopithecus reveal ring-shaped distributions of Fourier power at intermediate spatial frequencies, demonstrating a substantial nanostructure of the appropriate spatial frequency to produce the observed blue hues by coherent scattering alone. The Fourier power spectra and the observed reflectance spectra falsify assumptions and predictions of the incoherent, Rayleigh scattering hypothesis. Samples of blue Marmosa and Caluromys scrotum conform generally to the anatomy seen in Mandrillus and Cercopithecus but were not sufficiently well preserved to conduct numerical analyses. Colour-producing collagen arrays in mammals have evolved multiple times independently within the two clades of mammals known to have trichromatic colour vision. Mammalian colour-producing collagen arrays are anatomically and mechanistically identical to structures that have evolved convergently in the dermis of many lineages of birds, the tapetum of some mammals and the cornea of some fishes. These collagen arrays constitute quasi-ordered 2-D photonic crystals

Double scattering of light from biophotonic nanostructures with short-range order

We investigate the physical mechanism for color production by isotropic nanostructures with short-range order in bird feather barbs. While the primary peak in optical scattering spectra results from constructive interference of singly-scattered light, many species exhibit secondary peaks with distinct characteristic. Our experimental and numerical studies show that these secondary peaks result from double scattering of light by the correlated structures. Without an analog in periodic or random structures, such a phenomenon is unique for short-range ordered structures, and has been widely used by nature for non-iridescent structural coloration.Comment: 10 pages, 4 figure

Anatomically diverse butterfly scales all produce structural colours by coherent scattering

The structural colours of butterflies and moths (Lepidoptera) have been attributed to a diversity of physical mechanisms, including multilayer interference, diffraction, Bragg scattering, Tyndall scattering and Rayleigh scattering. We used fibre optic spectrophotometry, transmission electron microscopy (TEM) and 2D Fourier analysis to investigate the physical mechanisms of structural colour production in twelve lepidopteran species from four families, representing all of the previously proposed anatomical and optical classes of butterfly nanostructure. The 2D Fourier analyses of TEMs of colour producing butterfly scales document that all species are appropriately nanostructured to produce visible colours by coherent scattering, i.e. differential interference and reinforcement of scattered, visible wavelengths. Previously hypothesized to produce a blue colour by incoherent, Tyndall scattering, the scales of Papilio zalmoxis are not appropriately nanostructured for incoherent scattering. Rather, available data indicate that the blue of P. zalmoxis is a fluorescent pigmentary colour. Despite their nanoscale anatomical diversity, all structurally coloured butterfly scales share a single fundamental physical color production mechanism coherent scattering. Recognition of this commonality provides a new perspective on how the nanostructure and optical properties of structurally coloured butterfly scales evolved and diversified among and within lepidopteran clades

Blue integumentary structural colours in dragonflies (Odonata) are not produced by incoherent Tyndall scattering

For nearly 80 years, the non-iridescent, blue, integumentary structural colours of dragonflies and damselflies (Odonata) have been attributed to incoherent Tyndall or Rayleigh scattering. We investigated the production of the integumentary structural colours of a damselfly - the familiar bluet, Enallagma civile (Coenagrionidae) - and a dragonfly - the common green darner, Anax junius (Aeshnidae) - using fibre optic spectrophotometry and transmission electron microscopy (TEM). The reflectance spectra of both species showed discrete reflectance peaks of similar to30% reflectance at 475 and 460 nm, respectively. These structural colours are produced by light scattering from closely packed arrays of spheres in the endoplasmic reticulum of box-shaped epidermal pigment cells underlying the cuticle. The observed reflectance spectra do not conform to the inverse fourth power relationship predicted for Tyndall/Rayleigh scattering. Two-dimensional (2-D) Fourier analysis of the TEM images of the colour-producing arrays reveals ring-shaped distributions of Fourier power at intermediate spatial frequencies, documenting a quasiordered nanostructure. The nanostructured Fourier power spectra falsify the assumption of spatial independence of scatterers that is required for incoherent scattering. Radial averages of the Fourier power spectrum indicate that the spheres are substantially nanostructured at the appropriate spatial scale to produce visible colours by coherent scattering. However, the spatial periodicity of the arrays is apparently too large to produce the observed colour by coherent scattering. The nanospheres could have expanded substantially (similar to50%) during preparation for TEM. Alternatively, coherent light scattering could be occurring both from the surfaces and from structures at the centre of the spheres. These arrays of colour-producing spheres within pigment cells have convergently evolved at least 11-14 times independently within the Odonata. Structural colouration from arrays in living cells has also fostered the convergent evolution of temperature-dependent colour change in numerous odonate lineages

Structural absorption by barbule microstructures of super black bird of paradise feathers

Many studies have shown how pigments and internal nanostructures generate color in nature. External surface structures can also influence appearance, such as by causing multiple scattering of light (structural absorption) to produce a velvety, super black appearance. Here we show that feathers from five species of birds of paradise (Aves: Paradisaeidae) structurally absorb incident light to produce extremely low-reflectance, super black plumages. Directional reflectance of these feathers (0.05–0.31%) approaches that of man-made ultra-absorbent materials. SEM, nano-CT, and ray-tracing simulations show that super black feathers have titled arrays of highly modified barbules, which cause more multiple scattering, resulting in more structural absorption, than normal black feathers. Super black feathers have an extreme directional reflectance bias and appear darkest when viewed from the distal direction. We hypothesize that structurally absorbing, super black plumage evolved through sensory bias to enhance the perceived brilliance of adjacent color patches during courtship display

Coherent light scattering by nanostructured collagen arrays in the caruncles of the Malagasy asities (Eurylaimidae : Aves)

We investigated the anatomy, nanostructure and biophysics of the structurally coloured facial caruncles of three species in a clade of birds endemic to Madagascar (Philepittinae, Eurylaimidae: Aves), Caruncle tissues of all species had reflectance spectra with prominent, peak hues between 403 and 528 nm, Dark blue Neodrepanis tissues had substantial reflectance in the near ultraviolet (320-400 nm), which is visible to birds but not to humans, providing the first evidence of ultraviolet skin colours in birds and the first indications of the possible function of ultraviolet skin colours in avian communication, These structural colours are produced by coherent scattering from arrays of parallel collagen fibres in the dermis, Tissues of Philepitta castanea were organized into hexagonal, crystal-like arrays, whereas Neodrepanis tissues were quasiordered, Predictions of the peak hues of reflectance (lambda(max)) using Bragg's law were relatively accurate, but Bragg's law requires physical assumptions that are obviously violated by these structures. A two-dimensional discrete Fourier analysis of the spatial variation in refractive index within the tissues documented that all the tissues are substantially nanostructured at the appropriate spatial scale to scatter visible light coherently. Predicted reflectance spectra based on the two-dimensional Fourier power spectra are relatively accurate at predicting the hue and shape of the reflectance spectra of the tissues. These results confirm that the nanostructure of the collagen arrays determines the colours that are coherently scattered by these tissues, The evolution of the anatomy and nanostructure of asity caruncles is discussed

Molecular diversity, metabolic transformation, and evolution of carotenoid feather pigments in cotingas (Aves: Cotingidae)

Abstract Carotenoid pigments were extracted from 29 feather patches from 25 species of cotingas (Cotingidae) representing all lineages of the family with carotenoid plumage coloration. Using high-performance liquid chromatography (HPLC), mass spectrometry, chemical analysis, and 1 H-NMR, 16 different carotenoid molecules were documented in the plumages of the cotinga family. These included common dietary xanthophylls (lutein and zeaxanthin), canary xanthophylls A and B, four well known and broadly distributed avian ketocarotenoids (canthaxanthin, astaxanthin, a-doradexanthin, and adonixanthin), rhodoxanthin, and seven 4-methoxy-ketocarotenoids. Methoxy-ketocarotenoids were found in 12 species within seven cotinga genera, including a new, previously undescribed molecule isolated from the Andean Cock-of-the-Rock Rupicola peruviana, 3 0 -hydroxy-3-methoxy-b,b-carotene-4-one, which we name rupicolin. The diversity of cotinga plumage carotenoid pigments is hypothesized to be derived via four metabolic pathways from lutein, zeaxanthin, b-cryptoxanthin, and b-carotene. All metabolic transformations within the four pathways can be described by six or seven different enzymatic reactions. Three of these reactions are shared among three precursor pathways and are responsible for eight different metabolically derived carotenoid molecules. The function of cotinga plumage carotenoid diversity was analyzed with reflectance spectrophotometry of plumage patches and a tetrahedral model of avian color visual perception. The evolutionary history of the origin of this diversity is analyzed phylogenetically. The color space analyses document that the evolutionarily derived metabolic modifications of dietary xanthophylls have resulted in the creation of distinctive orange-red and purple visual colors