Evolution of single gyroid photonic crystals in bird feathers.

Vivid, saturated structural colors are conspicuous and important features of many animals. A rich diversity of three-dimensional periodic photonic nanostructures is found in the chitinaceous exoskeletons of invertebrates. Three-dimensional photonic nanostructures have been described in bird feathers, but they are typically quasi-ordered. Here, we report bicontinuous single gyroid ß-keratin and air photonic crystal networks in the feather barbs of blue-winged leafbirds (Chloropsis cochinchinensis sensu lato), which have evolved from ancestral quasi-ordered channel-type nanostructures. Self-assembled avian photonic crystals may serve as inspiration for multifunctional applications, as they suggest efficient, alternative routes to single gyroid synthesis at optical length scales, which has been experimentally elusive.

Genomic phylogeography of the White-crowned Manakin Pseudopipra pipra (Aves: Pipridae) illuminates a continental-scale radiation out of the Andes.

The complex landscape history of the Neotropics has generated opportunities for population isolation and diversification that place this region among the most species-rich in the world. Detailed phylogeographic studies are required to uncover the biogeographic histories of Neotropical taxa, to identify evolutionary correlates of diversity, and to reveal patterns of genetic connectivity, disjunction, and potential differentiation among lineages from different areas of endemism. The White-crowned Manakin (Pseudopipra pipra) is a small suboscine passerine bird that is broadly distributed through the subtropical rainforests of Central America, the lower montane cloud forests of the Andes from Colombia to central Peru, the lowlands of Amazonia and the Guianas, and the Atlantic forest of southeast Brazil. Pseudopipra is currently recognized as a single, polytypic biological species. We studied the effect of the Neotropical landscape on genetic and phenotypic differentiation within this species using genomic data derived from double digest restriction site associated DNA sequencing (ddRAD), and mitochondrial DNA. Most of the genetic breakpoints we identify among populations coincide with physical barriers to gene flow previously associated with avian areas of endemism. The phylogenetic relationships among these populations imply a novel pattern of Andean origination for this group, with subsequent diversification into the Amazonian lowlands. Our analysis of genomic admixture and gene flow reveals a complex history of introgression between some western Amazonian populations. These reticulate processes confound our application of standard concatenated and coalescent phylogenetic methods and raise the question of whether a lineage in the western Napo area of endemism should be considered a hybrid species. Lastly, analysis of variation in vocal and plumage phenotypes in the context of our phylogeny supports the hypothesis that Pseudopipra is a species-complex composed of at least 8, and perhaps up to 17 distinct species which have arisen in the last ~2.5 Ma.

Structural color from solid-state polymerization-induced phase separation.

Structural colors are produced by wavelength-dependent scattering of light from nanostructures. While living organisms often exploit phase separation to directly assemble structurally colored materials from macromolecules, synthetic structural colors are typically produced in a two-step process involving the sequential synthesis and assembly of building blocks. Phase separation is attractive for its simplicity, but applications are limited due to a lack of robust methods for its control. A central challenge is to arrest phase separation at the desired length scale. Here, we show that solid-state polymerization-induced phase separation can produce stable structures at optical length scales. In this process, a polymeric solid is swollen and softened with a second monomer. During its polymerization, the two polymers become immiscible and phase separate. As free monomer is depleted, the host matrix resolidifies and arrests coarsening. The resulting polymeric composites have a blue or white appearance. We compare these biomimetic nanostructures to those in structurally-colored feather barbs, and demonstrate the flexibility of this approach by producing structural color in filaments and large sheets.

A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing.

Although reconstruction of the phylogeny of living birds has progressed tremendously in the last decade, the evolutionary history of Neoaves--a clade that encompasses nearly all living bird species--remains the greatest unresolved challenge in dinosaur systematics. Here we investigate avian phylogeny with an unprecedented scale of data: >390,000 bases of genomic sequence data from each of 198 species of living birds, representing all major avian lineages, and two crocodilian outgroups. Sequence data were collected using anchored hybrid enrichment, yielding 259 nuclear loci with an average length of 1,523 bases for a total data set of over 7.8 × 10(7) bases. Bayesian and maximum likelihood analyses yielded highly supported and nearly identical phylogenetic trees for all major avian lineages. Five major clades form successive sister groups to the rest of Neoaves: (1) a clade including nightjars, other caprimulgiforms, swifts, and hummingbirds; (2) a clade uniting cuckoos, bustards, and turacos with pigeons, mesites, and sandgrouse; (3) cranes and their relatives; (4) a comprehensive waterbird clade, including all diving, wading, and shorebirds; and (5) a comprehensive landbird clade with the enigmatic hoatzin (Opisthocomus hoazin) as the sister group to the rest. Neither of the two main, recently proposed Neoavian clades--Columbea and Passerea--were supported as monophyletic. The results of our divergence time analyses are congruent with the palaeontological record, supporting a major radiation of crown birds in the wake of the Cretaceous-Palaeogene (K-Pg) mass extinction.

Structurally assisted super black in colourful peacock spiders.

Male peacock spiders ( Maratus, Salticidae) compete to attract female mates using elaborate, sexually selected displays. They evolved both brilliant colour and velvety black. Here, we use scanning electron microscopy, hyperspectral imaging and finite-difference time-domain optical modelling to investigate the deep black surfaces of peacock spiders. We found that super black regions reflect less than 0.5% of light (for a 30° collection angle) in Maratus speciosus (0.44%) and Maratus karrie (0.35%) owing to microscale structures. Both species evolved unusually high, tightly packed cuticular bumps (microlens arrays), and M. karrie has an additional dense covering of black brush-like scales atop the cuticle. Our optical models show that the radius and height of spider microlenses achieve a balance between (i) decreased surface reflectance and (ii) enhanced melanin absorption (through multiple scattering, diffraction out of the acceptance cone of female eyes and increased path length of light through absorbing melanin pigments). The birds of paradise (Paradiseidae), ecological analogues of peacock spiders, also evolved super black near bright colour patches. Super black locally eliminates white specular highlights, reference points used to calibrate colour perception, making nearby colours appear brighter, even luminous, to vertebrates. We propose that this pre-existing, qualitative sensory experience-'sensory bias'-is also found in spiders, leading to the convergent evolution of super black for mating displays in jumping spiders.

Female resistance to sexual coercion can evolve to preserve the indirect benefits of mate choice.

Sexual conflict over the indirect benefits of mate choice may arise when traits in one sex limit the ability of the other sex to freely choose mates but when these coercive traits are not necessarily directly harmful (i.e. forced fertilization per se). Although we might hypothesize that females can evolve resistance in order to retain the indirect, genetic benefits (reflected in offspring attractiveness) of mating with attractive males, up to now it has been difficult to evaluate potential underlying mechanisms. Traditional theoretical approaches do not usually conceptually distinguish between female preference for male mating display and female resistance to forced fertilization, yet sexual conflict over indirect benefits implies the simultaneous action of all of these traits. Here, we present an integrative theoretical framework that draws together concepts from both sexual selection and sexual conflict traditions, allowing for the simultaneous coevolution of displays and preferences, and of coercion and resistance. We demonstrate that it is possible for resistance to coercion to evolve in the absence of direct costs of mating to preserve the indirect benefits of mate choice. We find that resistance traits that improve the efficacy of female mating preference can evolve as long as females are able to attain some indirect benefits of mating with attractive males, even when both attractive and unattractive males can coerce. These results reveal new evolutionary outcomes that were not predicted by prior theories of indirect benefits or sexual conflict.

Convergent evolution of super black plumage near bright color in 15 bird families.

We examined extremely low-reflectance, velvety black plumage patches in 32 bird species from 15 families and five orders and compared them with 22 closely related control species with normal black plumage. We used scanning electron microscopy to investigate microscopic feather anatomy, and applied spectrophotometry and hyperspectral imaging to measure plumage reflectance. Super black plumages are significantly darker and have more broadband low reflectance than normal black plumages, and they have evolved convergently in 15 avian families. Super black feather barbules quantitatively differ in microstructure from normal black feathers. Microstructural variation is significantly correlated with reflectance: tightly packed, strap-shaped barbules have lower reflectance. We assigned these super black feathers to five heuristic classes of microstructure, each of which has evolved multiple times independently. All classes have minimal exposed horizontal surface area and 3D micrometer-scale cavities greater in width and depth than wavelengths of light. In many species, barbule morphology varied between the super black exposed tip of a feather and its (i) concealed base or (ii) iridescently colored spot. We propose that super black plumages reduce reflectance, and flatten reflectance spectra, through multiple light scattering between the vertically oriented surfaces of microscale cavities, contributing to near-complete absorption of light by melanin. All super black plumage patches identified occur adjacent to brilliant colored patches. Super black plumage lacks all white specular reflections (reference points used to calibrate color perception), thus exaggerating the perceived brightness of nearby colors. We hypothesize that this sensory bias is an unavoidable by-product of color correction in variable light environments.

Mimicry Cycles, Traps, and Chains: The Coevolution of Toucan and Kiskadee Mimicry.

Interspecific social dominance mimicry (ISDM) is a form of social parasitism in which a subordinate species evolves to mimic and deceive a dominant interference competitor in order to avoid attack by the dominant species. ISDM has been proposed to result in (1) antagonistic coevolutionary arms races in appearance between the model and the mimic (e.g., Ramphastos toucans) and (2) the evolution of complexes of multiple species converging on a common visual appearance (e.g., kiskadee flycatchers). We present evolutionary games of antagonistic coevolution in appearance between pairs and triplets of sympatric species under interference competition. We identify conditions for the existence and stability of (1) coevolutionary mimicry cycles in appearance between evader and pursuer strategies of models and mimics, (2) mimicry chains in which three or more species are coevolutionarily entrained to evolve a single common appearance despite differences in their costs and benefits, and (3) mimicry traps in which a subdominant species is evolutionarily constrained from evading mimicry by a third, subordinate mimic species. Mimicry cycles will result in the evolutionary divergence of models and mimics from their ancestral phenotypes. The hierarchical evolutionary dynamics of ISDM traps and chains resemble Müllerian mimicry with variable costs to toxicity.

Smithornis broadbills produce loud wing song by aeroelastic flutter of medial primary wing feathers.

Broadbills in the genus Smithornis produce a loud brreeeeet during a distinctive flight display. It has been posited that this klaxon-like sound is generated non-vocally with the outer wing feathers (P9, P10), but no scientific studies have previously addressed this hypothesis. Although most birds that make non-vocal communication sounds have feathers with a shape distinctively modified for sound production, Smithornis broadbills do not. We investigated whether this song is produced vocally or with the wings in rufous-sided broadbill (S. rufolateralis) and African broad bill (S. capensis). In support of the wing song hypothesis, synchronized high-speed video and sound recordings of displays demonstrated that sound pulses were produced during the downstroke, subtle gaps sometimes appeared between the outer primary feathers P6-P10, and wing tip speed reached 16 m s(-1) Tests of a spread wing in a wind tunnel demonstrated that at a specific orientation, P6 and P7 flutter and produce sound. Wind tunnel tests on individual feathers P5-P10 from a male of each species revealed that while all of these feathers can produce sound via aeroelastic flutter, P6 and P7 produce the loudest sounds, which are similar in frequency to the wing song, at airspeeds achievable by the wing tip during display flight. Consistent with the wind tunnel experiments, field manipulations of P6, P7 and P8 changed the timbre of the wing song, and reduced its tonality, demonstrating that P6 and P7 are together the sound source, and not P9 or P10. The resultant wing song appears to have functionally replaced vocal song.

Moulting tail feathers in a juvenile oviraptorisaur.

Xu et al. describe the extraordinarily preserved feathers from two subadults of the oviraptorisaur Similicaudipteryx from the Yixian Formation of Liaoning, China. The preserved tail feathers of the juvenile specimen (STM4.1) show a morphology not previously observed in any fossil feathers. The tail feathers of an older, immature specimen (STM22-6) show a typical closed pennaceous structure with a prominent, planar vane. I propose that the feathers of the tail of the juvenile specimen are not a specialized feather generation, but fossilized 'pin feathers' or developing feather germs.

Structural Diversity of Arthropod Biophotonic Nanostructures Spans Amphiphilic Phase-Space.

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.

Nuclear ß-catenin localization supports homology of feathers, avian scutate scales, and alligator scales in early development.

Feathers are an evolutionary novelty found in all extant birds. Despite recent progress investigating feather development and a revolution in dinosaur paleontology, the relationship of feathers to other amniote skin appendages, particularly reptile scales, remains unclear. Disagreement arises primarily from the observation that feathers and avian scutate scales exhibit an anatomical placode-defined as an epidermal thickening-in early development, whereas alligator and other avian scales do not. To investigate the homology of feathers and archosaur scales we examined patterns of nuclear ß-catenin localization during early development of feathers and different bird and alligator scales. In birds, nuclear ß-catenin is first localized to the feather placode, and then exhibits a dynamic pattern of localization in both epidermis and dermis of the feather bud. We found that asymmetric avian scutate scales and alligator scales share similar patterns of nuclear ß-catenin localization with feathers. This supports the hypothesis that feathers, scutate scales, and alligator scales are homologous during early developmental stages, and are derived from early developmental stages of an asymmetric scale present in the archosaur ancestor. Furthermore, given that the earliest stage of ß-catenin localization in feathers and archosaur scales is also found in placodes of several mammalian skin appendages, including hair and mammary glands, we hypothesize that a common skin appendage placode originated in the common ancestor of all amniotes. We suggest a skin placode should not be defined by anatomical features, but as a local, organized molecular signaling center from which an epidermal appendage develops.

Barb geometry of asymmetrical feathers reveals a transitional morphology in the evolution of avian flight.

The geometry of feather barbs (barb length and barb angle) determines feather vane asymmetry and vane rigidity, which are both critical to a feather's aerodynamic performance. Here, we describe the relationship between barb geometry and aerodynamic function across the evolutionary history of asymmetrical flight feathers, from Mesozoic taxa outside of modern avian diversity (Microraptor, Archaeopteryx, Sapeornis, Confuciusornis and the enantiornithine Eopengornis) to an extensive sample of modern birds. Contrary to previous assumptions, we find that barb angle is not related to vane-width asymmetry; instead barb angle varies with vane function, whereas barb length variation determines vane asymmetry. We demonstrate that barb geometry significantly differs among functionally distinct portions of flight feather vanes, and that cutting-edge leading vanes occupy a distinct region of morphospace characterized by small barb angles. This cutting-edge vane morphology is ubiquitous across a phylogenetically and functionally diverse sample of modern birds and Mesozoic stem birds, revealing a fundamental aerodynamic adaptation that has persisted from the Late Jurassic. However, in Mesozoic taxa stemward of Ornithurae and Enantiornithes, trailing vane barb geometry is distinctly different from that of modern birds. In both modern birds and enantiornithines, trailing vanes have larger barb angles than in comparatively stemward taxa like Archaeopteryx, which exhibit small trailing vane barb angles. This discovery reveals a previously unrecognized evolutionary transition in flight feather morphology, which has important implications for the flight capacity of early feathered theropods such as Archaeopteryx and Microraptor. Our findings suggest that the fully modern avian flight feather, and possibly a modern capacity for powered flight, evolved crownward of Confuciusornis, long after the origin of asymmetrical flight feathers, and much later than previously recognized.

Diversity, physiology, and evolution of avian plumage carotenoids and the role of carotenoid-protein interactions in plumage color appearance.

The diversity of vibrant plumage colors in birds has evolved as a direct result of social and environmental pressures. To fully understand these underlying pressures it is necessary to elucidate the mechanisms for the creation of novel plumage colors which include the metabolic transformations of dietary carotenoids and spectral tuning of the molecules within the feather protein environment. Recent advances in this field have greatly expanded the number and breadth of avian species for which plumage pigmentation has been characterized, making it possible to reconstruct the phylogenetic history of carotenoid usage in plumage. Resonance Raman and classical Raman spectroscopic techniques have been employed with great effect in the study of carotenoids in situ. The application of these methods have two benefits: to identify carotenoids in feathers that are unavailable for destructive sampling; and to study the spectral tuning resulting from the interaction between the carotenoids and the proteins to which they are bound. This review presents a summary of recent advances in the understanding of the molecular factors controlling the coloration of avian carotenoid plumage obtained through the application of both bioanalytical and spectroscopic methodologies.

Aeroelastic flutter of feathers, flight and the evolution of non-vocal communication in birds.

Tonal, non-vocal sounds are widespread in both ordinary bird flight and communication displays. We hypothesized these sounds are attributable to an aerodynamic mechanism intrinsic to flight feathers: aeroelastic flutter. Individual wing and tail feathers from 35 taxa (from 13 families) that produce tonal flight sounds were tested in a wind tunnel. In the wind tunnel, all of these feathers could flutter and generate tonal sound, suggesting that the capacity to flutter is intrinsic to flight feathers. This result implies that the aerodynamic mechanism of aeroelastic flutter is potentially widespread in flight of birds. However, the sounds these feathers produced in the wind tunnel replicated the actual flight sounds of only 15 of the 35 taxa. Of the 20 negative results, we hypothesize that 10 are false negatives, as the acoustic form of the flight sound suggests flutter is a likely acoustic mechanism. For the 10 other taxa, we propose our negative wind tunnel results are correct, and these species do not make sounds via flutter. These sounds appear to constitute one or more mechanism(s) we call 'wing whirring', the physical acoustics of which remain unknown. Our results document that the production of non-vocal communication sounds by aeroelastic flutter of flight feathers is widespread in birds. Across all birds, most evolutionary origins of wing- and tail-generated communication sounds are attributable to three mechanisms: flutter, percussion and wing whirring. Other mechanisms of sound production, such as turbulence-induced whooshes, have evolved into communication sounds only rarely, despite their intrinsic ubiquity in ordinary flight.

Theoretical morphology and development of flight feather vane asymmetry with experimental tests in parrots.

Asymmetry in flight feather vane width is a major functional innovation associated with the evolution of flight in the ancestors of birds. However, the developmental and morphological basis of feather shape is not simple, and the developmental processes involved in vane width asymmetry are poorly understood. We present a theoretical model of feather morphology and development that describes the possible ways to modify feather development and produce vane asymmetry. Our model finds that the theoretical morphospace of feather shape is redundant, and that many different combinations of parameters could be responsible for vane asymmetry in a given feather. Next, we empirically measured morphological and developmental model parameters in asymmetric and symmetric feathers from two species of parrots to identify which combinations of parameters create vane asymmetry in real feathers. We found that both longer barbs, and larger barb angles in the relatively wider trailing vane drove asymmetry in tail feathers. Developmentally, longer barbs were the result of an offset of the radial position of the new barb locus, whereas larger barb angles were produced by differential expansion of barbs as the feather unfurls from the tubular feather germ. In contrast, the helical angle of barb ridge development did not contribute to vane asymmetry and could be indicative of a constraint. This research provides the first comprehensive description of both the morphological and developmental modifications responsible for vane asymmetry within real feathers, and identifies key steps that must have occurred during the evolution of vane asymmetry.

A comprehensive multilocus phylogeny of the Neotropical cotingas (Cotingidae, Aves) with a comparative evolutionary analysis of breeding system and plumage dimorphism and a revised phylogenetic classification.

The Neotropical cotingas (Cotingidae: Aves) are a group of passerine birds that are characterized by extreme diversity in morphology, ecology, breeding system, and behavior. Here, we present a comprehensive phylogeny of the Neotropical cotingas based on six nuclear and mitochondrial loci (∼7500 bp) for a sample of 61 cotinga species in all 25 genera, and 22 species of suboscine outgroups. Our taxon sample more than doubles the number of cotinga species studied in previous analyses, and allows us to test the monophyly of the cotingas as well as their intrageneric relationships with high resolution. We analyze our genetic data using a Bayesian species tree method, and concatenated Bayesian and maximum likelihood methods, and present a highly supported phylogenetic hypothesis. We confirm the monophyly of the cotingas, and present the first phylogenetic evidence for the relationships of Phibalura flavirostris as the sister group to Ampelion and Doliornis, and the paraphyly of Lipaugus with respect to Tijuca. In addition, we resolve the diverse radiations within the Cotinga, Lipaugus, Pipreola, and Procnias genera. We find no support for Darwin's (1871) hypothesis that the increase in sexual selection associated with polygynous breeding systems drives the evolution of color dimorphism in the cotingas, at least when analyzed at a broad categorical scale. Finally, we present a new comprehensive phylogenetic classification of all cotinga species.

How colorful are fruits? Limited color diversity in fleshy fruits on local and global scales.

The colors of fleshy fruits are considered to be a signal to seed-dispersing animals, but their diversity remains poorly understood. Using an avian color space to derive a sensory morphospace for fruit color, we tested four hypotheses of fruit color diversity: fruit colors occupy a limited area of the color space; they are less diverse than flower colors; fruit colors within localities are similar to each other; and fruit color diversity reflects phylogeny. The global fruit color diversity of 948 primarily bird-dispersed plant species and the color diversity of localities were compared with null models of random, unconstrained evolution of fruit color. Fruit color diversity was further compared with the diversity of 1300 flower colors. Tests of phylogenetic effects on fruit color were used to assess the degree of correspondence with phylogeny. Global and local fruit color diversity was limited compared with null models and fruits have achieved only half the color diversity of flowers. Interestingly, we found little indication of phylogenetic conservatism. Constraints resulting from the chemical properties of pigments probably limit global fruit and flower color diversity. Different types of selection on fruits and flowers may further explain the smaller color diversity of fruits.

Carotenoids from the crimson and maroon plumages of Old World orioles (Oriolidae).

Recent analyses of the orange, red, and purple plumages of cotingas (Cotingidae) and broadbills (Eurylaimidae) revealed the presence of novel carotenoid molecules, suggesting that the diversity of pigments and the metabolic transformations they undergo are not yet fully understood. Two Old World orioles, the Black-and-Crimson Oriole Oriolus cruentus, and the Maroon Oriole Oriolus traillii, exhibit plumage colors that are similar to those of some cotingas and broadbills. To determine if these oriole plumage colors are produced by the same carotenoids or with other molecules, we used high-performance liquid chromatography (HPLC), mass spectrometry, and chemical analyses. The data show that the bright red feathers of O. cruentus contain a suite of keto-carotenoids commonly found in avian plumages, including canthaxanthin, adonirubin, astaxanthin, papilioerythrinone, and α-doradexanthin. The maroon feathers of O. traillii were found to contain canthaxanthin, α-doradexanthin, and one novel carotenoid, 3',4-dihydroxy-ε,ε-carotene-3-one, which we have termed "4-hydroxy-canary xanthophyll A." In this paper we propose the metabolic pathways by which these pigments are formed. This work advances our understanding of the evolution of carotenoid metabolism in birds and the mechanisms by which birds achieve their vivid plumage colorations.

Nuclear magnetic resonance analysis of carotenoids from the burgundy plumage of the Pompadour Cotinga (Xipholena punicea).

Previous analysis of carotenoids extracted from the burgundy plumage of the Pompadour Cotinga (Xipholena punicea) revealed six novel keto-carotenoid pigments with methoxyl groups in the C3-position of one or both ß-rings. High performance liquid chromatography (HPLC), mass spectrometry, chemical analysis and, in some instances (1)H NMR spectroscopy were employed to determine the structures of the molecules. Further analysis by NMR was precluded due to lack of material. The recent acquisition of multiple feathers from X. punicea specimens has made it possible to complete this work using correlated homonuclear spectroscopy (COSY), nuclear overhauser effect spectroscopy (NOESY) and (1)H NMR. These new data conclusively confirm the structures of the six methoxy-carotenoids suggested by the earlier work. In addition, the resonance positions of the protons from the novel 3-methoxy-4-keto-ß-ring and 2,3-didehydro-3-methoxy-4-keto-ß-ring moieties are reported here for the first time.