SOCIAL CONTEXT AND THE EVOLUTION OF DELAYED REPRODUCTION IN BIRDS.

Classic life history theory makes generalized predictions about phenotypic correlations across large clades. Modern comparative tests of these correlations account for the underlying structure of phylogenetic trees. Yet neither life history theory nor phylogenetic comparative methods automatically specify how biological mechanisms generate correlations. This problem is evident in comparative analyses of birds. Birds show a correlation between body size and age at first reproduction, but do not actually grow larger if they delay reproduction. Instead, field studies raise the hypothesis that social contexts-especially cooperative breeding, coloniality, and lekking-generate unique demands for behavioral development, which in turn result in delayed reproduction. Here, we support that hypothesis with a comparative dataset spanning 961 species in 155 avian families. Continuous (Ornstein-Uhlenbeck), discrete (hidden state Markov), and phylogenetic regression models revealed delayed reproduction in colonial birds, a weaker signal in cooperative birds, and the consistent evolution of sexual bimaturism in polygynous, lekking birds. These results show an association between diverse social contexts, sex-specific developmental demands, and life history evolution in birds. Considering this diversity, we discuss how even statistically powerful phylogenetic correlations-whether focused on mass, lifespan, or broad social categories-can ultimately fail to model the history of life history evolution.

Remodeling male coercion and the evolution of sexual autonomy by mate choice.

Models of sexual conflict over mating, including conflict over indirect benefits of mate choice, have generally presumed that female resistance to male coercion must involve direct confrontation, which can lead to sexually antagonistic coevolutionary arms-races. We built a quantitative model examining the largely ignored possibility that females may evolve new, additional mate preferences for new male traits that undermine male capacity to coerce. Thus, females may "remodel" the coercive capacity of the male phenotype in order to enhance their own sexual autonomy-a novel alternative mechanism by which females may avoid arms-races. We demonstrate that evolutionary "remodeling" is possible, in spite of costs to males, because females that prefer males with protective, autonomy-enhancing traits (traits correlated with lower coercion effectiveness) are likelier to gain indirect benefits of having attractive mates. Our analysis reveals new possibilities for the evolution of systems of sexual conflict over indirect benefits, showing that autonomy-enhancing male traits can act as a "public good," benefiting all females regardless of mating preferences, leading to oscillatory dynamics; and that preferences for more protective male traits will often be favored relative to preferences for less protective traits, potentially leading to an evolutionary "snowball" of expanding sexual autonomy.

Hummingbird plumage color diversity exceeds the known gamut of all other birds.

A color gamut quantitatively describes the diversity of a taxon's integumentary coloration as seen by a specific organismal visual system. We estimated the plumage color gamut of hummingbirds (Trochilidae), a family known for its diverse barbule structural coloration, using a tetrahedral avian color stimulus space and spectra from a taxonomically diverse sample of 114 species. The spectra sampled occupied 34.2% of the total diversity of colors perceivable by hummingbirds, which suggests constraints on their plumage color production. However, the size of the hummingbird color gamut is equivalent to, or greater than, the previous estimate of the gamut for all birds. Using the violet cone type visual system, our new data for hummingbirds increases the avian color gamut by 56%. Our results demonstrate that barbule structural color is the most evolvable plumage coloration mechanism, achieving unique, highly saturated colors with multi-reflectance peaks.

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.

Constraint and Function in the Predefinitive Plumages of Manakins (Aves: Pipridae).

Birds with delayed plumage maturation exhibit a drab predefinitive plumage, often despite gonad maturation, before developing the definitive plumage associated with increased reproductive success. Manakins are a diverse clade of neotropical lekking birds with extreme sexual dichromatism, radical sexual displays, and a unique diversity in the predefinitive plumages of males across species. Here, we provide the first full review of the natural history of manakin predefinitive plumages as the basis for qualitatively addressing the six major hypotheses about the production and function of predefinitive plumages. We find little evidence to support the possibilities that manakin predefinitive plumages are directly constrained by inflexible molt schedules, resource limitations to definitive coloration, or hormonal ties to reproductive behaviors. There is little evidence that could support a crypsis function, although direct experimentation is needed, and mimicry is refuted except for one unusual species in which predefinitive males sire young. Instead, evidence from a handful of well-studied species suggests that predefinitive plumages help young males explicitly signal their social status, and thereby gain entry to the social hierarchies which dictate future reproductive success. Our conclusions are especially influenced by the unique fact that males of at least 11 species throughout the family exhibit multiple predefinitive plumage stages with distinctively male patches. For each hypothesis, we highlight ways in which a better knowledge of female and young male birds offers critical opportunities for the use of manakins as a model clade.

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.

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.

Higher-Order Musical Temporal Structure in Bird Song.

Bird songs often display musical acoustic features such as tonal pitch selection, rhythmicity, and melodic contouring. We investigated higher-order musical temporal structure in bird song using an experimental method called "music scrambling" with human subjects. Recorded songs from a phylogenetically diverse group of 20 avian taxa were split into constituent elements ("notes" or "syllables") and recombined in original and random order. Human subjects were asked to evaluate which version sounded more "musical" on a per-species basis. Species identity and stimulus treatment were concealed from subjects, and stimulus presentation order was randomized within and between taxa. Two recordings of human music were included as a control for attentiveness. Participants varied in their assessments of individual species musicality, but overall they were significantly more likely to rate bird songs with original temporal sequence as more musical than those with randomized temporal sequence. We discuss alternative hypotheses for the origins of avian musicality, including honest signaling, perceptual bias, and arbitrary aesthetic coevolution.

Expanding the eggshell colour gamut: uroerythrin and bilirubin from tinamou (Tinamidae) eggshells.

To date, only two pigments have been identified in avian eggshells: rusty-brown protoporphyrin IX and blue-green biliverdin IXα. Most avian eggshell colours can be produced by a mixture of these two tetrapyrrolic pigments. However, tinamou (Tinamidae) eggshells display colours not easily rationalised by combination of these two pigments alone, suggesting the presence of other pigments. Here, through extraction, derivatization, spectroscopy, chromatography, and mass spectrometry, we identify two novel eggshell pigments: yellow-brown tetrapyrrolic bilirubin from the guacamole-green eggshells of Eudromia elegans, and red-orange tripyrrolic uroerythrin from the purplish-brown eggshells of Nothura maculosa. Both pigments are known porphyrin catabolites and are found in the eggshells in conjunction with biliverdin IXα. A colour mixing model using the new pigments and biliverdin reproduces the respective eggshell colours. These discoveries expand our understanding of how eggshell colour diversity is achieved. We suggest that the ability of these pigments to photo-degrade may have an adaptive value for the tinamous.

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.

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.

Complex coevolution of wing, tail, and vocal sounds of courting male bee hummingbirds.

Phenotypic characters with a complex physical basis may have a correspondingly complex evolutionary history. Males in the "bee" hummingbird clade court females with sound from tail-feathers, which flutter during display dives. On a phylogeny of 35 species, flutter sound frequency evolves as a gradual, continuous character on most branches. But on at least six internal branches fall two types of major, saltational changes: mode of flutter changes, or the feather that is the sound source changes, causing frequency to jump from one discrete value to another. In addition to their tail "instruments," males also court females with sound from their syrinx and wing feathers, and may transfer or switch instruments over evolutionary time. In support of this, we found a negative phylogenetic correlation between presence of wing trills and singing. We hypothesize this transference occurs because wing trills and vocal songs serve similar functions and are thus redundant. There are also three independent origins of self-convergence of multiple signals, in which the same species produces both a vocal (sung) frequency sweep, and a highly similar nonvocal sound. Moreover, production of vocal, learned song has been lost repeatedly. Male bee hummingbirds court females with a diverse, coevolving array of acoustic traits.

Pervasive Correlated Evolution in Gene Expression Shapes Cell and Tissue Type Transcriptomes.

The evolution and diversification of cell types is a key means by which animal complexity evolves. Recently, hierarchical clustering and phylogenetic methods have been applied to RNA-seq data to infer cell type evolutionary history and homology. A major challenge for interpreting this data is that cell type transcriptomes may not evolve independently due to correlated changes in gene expression. This nonindependence can arise for several reasons, such as common regulatory sequences for genes expressed in multiple tissues, that is, pleiotropic effects of mutations. We develop a model to estimate the level of correlated transcriptome evolution (LCE) and apply it to different data sets. The results reveal pervasive correlated transcriptome evolution among different cell and tissue types. In general, tissues related by morphology or developmental lineage exhibit higher LCE than more distantly related tissues. Analyzing new data collected from bird skin appendages suggests that LCE decreases with the phylogenetic age of tissues compared, with recently evolved tissues exhibiting the highest LCE. Furthermore, we show correlated evolution can alter patterns of hierarchical clustering, causing different tissue types from the same species to cluster together. To identify genes that most strongly contribute to the correlated evolution signal, we performed a gene-wise estimation of LCE on a data set with ten species. Removing genes with high LCE allows for accurate reconstruction of evolutionary relationships among tissue types. Our study provides a statistical method to measure and account for correlated gene expression evolution when interpreting comparative transcriptome data.

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.

The biology of color.

Coloration mediates the relationship between an organism and its environment in important ways, including social signaling, antipredator defenses, parasitic exploitation, thermoregulation, and protection from ultraviolet light, microbes, and abrasion. Methodological breakthroughs are accelerating knowledge of the processes underlying both the production of animal coloration and its perception, experiments are advancing understanding of mechanism and function, and measurements of color collected noninvasively and at a global scale are opening windows to evolutionary dynamics more generally. Here we provide a roadmap of these advances and identify hitherto unrecognized challenges for this multi- and interdisciplinary field.

Domain morphology, boundaries, and topological defects in biophotonic gyroid nanostructures of butterfly wing scales.

Many organisms in nature have evolved sophisticated cellular mechanisms to produce photonic nanostructures and, in recent years, diverse crystalline symmetries have been identified and related to macroscopic optical properties. However, because we know little about the distributions of domain sizes, the orientations of photonic crystals, and the nature of defects in these structures, we are unable to make the connection between the nanostructure and its development and functionality. We report on nondestructive studies of the morphology of chitinous photonic crystals in butterfly wing scales. Using spatially and angularly resolved x-ray diffraction, we find that the domains are highly oriented with respect to the whole scale, indicating growth from scale boundaries. X-ray coherent diffractive imaging reveals two types of crystalline domain interfaces: abrupt changes between domains emerging from distinct nucleation sites and smooth transitions with edge dislocations presumably resulting from internal stresses during nanostructure development. Our study of the scale structure reveals new aspects of photonic crystal growth in butterfly wings and shows their similarity to block copolymer materials. It opens new avenues to exploration of fundamental processes underlying the growth of biological photonic nanostructures in a variety of species.

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.

Theory of the development of curved barbs and their effects on feather morphology.

Feathers exhibit an extraordinary diversity of shapes, which are used by birds to accomplish a diverse set of functions. Pennaceous feathers have a double branched morphology that develops from a tube of epidermis, and variation in branch geometry determines feather shape. Feather development is both complex (i.e., a simple developmental modification can have multiple effects on mature feather shape), and redundant (i.e., different developmental modifications can create the same shape). Due to this, it is not readily apparent how different feather shapes develop. In many feathers, barbs are not straight, but instead curve in toward, or away, from the feather tip. Barb curvature can affect the shape of mature feathers but the development of curved barbs is unknown. Previous research has hypothesized that barb curvature could develop either during the helical growth of barb ridges in the tubular feather germ, or during barb angle expansion as the feather unfurls from the sheath. To better understand the development of curved barbs and their effects on mature feathers we present a theoretical model of curved barb development and test the model with empirical investigations of feathers. We find that curved barbs affect many aspects of feather morphology including vane width, barb length, and barb spacing. In real feathers, curved barbs can develop both during helical barb ridge growth and during barb angle expansion, with most of the observed curvature due to barb angle expansion. Our results demonstrate that barb angle expansion as a feather unfurls from the sheath is a complex and dynamic process that plays an important role in determining the shape and structure of mature feathers. Curved barbs create heterogeneity in barb geometry within the feather vane, which could have important implications for aerodynamic function and the development of within feather pigmentation patterns. J. Morphol. 277:995-1013, 2016. © 2016 Wiley Periodicals, Inc.

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.