Homology and the evolution of vocal folds in the novel avian voice box.

The origin of novel traits, those that are not direct modifications of a pre-existing ancestral structure, remains a fundamental problem in evolutionary biology. For example, little is known about the evolutionary and developmental origins of the novel avian vocal organ, the syrinx. Located at the tracheobronchial junction, the syrinx is responsible for avian vocalization, but it is unclear whether avian vocal folds are homologous to the laryngeal vocal folds in other tetrapods or convergently evolved. Here, we identify a core developmental program involved in avian vocal fold formation and infer the morphology of the syrinx of the ancestor of modern birds. We find that this ancestral syrinx had paired sound sources induced by a conserved developmental pathway and show that shifts in these signals correlate with syringeal diversification. We show that, despite being derived from different developmental tissues, vocal folds in the syrinx and larynx have similar tissue composition and are established through a strikingly similar developmental program, indicating that co-option of an ancestral developmental program facilitated the origin of vocal folds in the avian syrinx.

Genomic signatures of convergent shifts to plunge-diving behavior in birds.

Understanding the genetic basis of convergence at broad phylogenetic scales remains a key challenge in biology. Kingfishers (Aves: Alcedinidae) are a cosmopolitan avian radiation with diverse colors, diets, and feeding behaviors-including the archetypal plunge-dive into water. Given the sensory and locomotor challenges associated with air-water transitions, kingfishers offer a powerful opportunity to explore the effects of convergent behaviors on the evolution of genomes and phenotypes, as well as direct comparisons between continental and island lineages. Here, we use whole-genome sequencing of 30 diverse kingfisher species to identify the genomic signatures associated with convergent feeding behaviors. We show that species with smaller ranges (i.e., on islands) have experienced stronger demographic fluctuations than those on continents, and that these differences have influenced the dynamics of molecular evolution. Comparative genomic analyses reveal positive selection and genomic convergence in brain and dietary genes in plunge-divers. These findings enhance our understanding of the connections between genotype and phenotype in a diverse avian radiation.

Complex plumages spur rapid color diversification in kingfishers (Aves: Alcedinidae).

Colorful signals in nature provide some of the most stunning examples of rapid phenotypic evolution. Yet, studying color pattern evolution has been historically difficult owing to differences in perceptual ability of humans and analytical challenges with studying how complex color patterns evolve. Island systems provide a natural laboratory for testing hypotheses about the direction and magnitude of phenotypic change. A recent study found that plumage colors of island species are darker and less complex than continental species. Whether such shifts in plumage complexity are associated with increased rates of color evolution remains unknown. Here, we use geometric morphometric techniques to test the hypothesis that plumage complexity and insularity interact to influence color diversity in a species-rich clade of colorful birds-kingfishers (Aves: Alcedinidae). In particular, we test three predictions: (1) plumage complexity enhances interspecific rates of color evolution, (2) plumage complexity is lower on islands, and (3) rates of plumage color evolution are higher on islands. Our results show that more complex plumages result in more diverse colors among species and that island species have higher rates of color evolution. Importantly, we found that island species did not have more complex plumages than their continental relatives. Thus, complexity may be a key innovation that facilitates evolutionary response of individual color patches to distinct selection pressures on islands, rather than being a direct target of selection itself. This study demonstrates how a truly multivariate treatment of color data can reveal evolutionary patterns that might otherwise go unnoticed.

Birds are among the most colorful animals on Earth. The different patterns and colors displayed on their feathers help them to identify their own species, attract mates or hide from predators. The bright plumages of birds are achieved through either pigments (such as reds and yellows) or structures (such as blues, greens or ultraviolet) inside feathers, or through a combination of both pigments and structures. Variation in the diversity of color patterns over time can give a helpful insight into the rate of evolution of a species. For example, structural colors evolve more quickly than pigment-based ones and can therefore be a key feature involved in species recognition or mate attraction. Studying the evolution of plumage patterns has been challenging due to differences in the vision of humans and birds. However, recent advances in technology have enabled researchers to map the exact wavelengths of the colors that make up the patterns, allowing for rigorous comparison of plumage color patterns across different individuals and species. To gain a greater understanding of how plumage color patterns evolve in birds, Eliason et al. studied kingfishers, a group of birds known for their complex and variable color patterns, and their worldwide distribution. The experiments analyzed the plumage color patterns of 72 kingfisher species (142 individual museum specimens) from both mainland and island populations by quantifying the amount of different wavelengths of light reflecting from a feather and accounting for relationships among species and among feather patches. The analyzes showed that having more complex patterns leads to a greater accumulation of plumage colors over time, supporting the idea that complex plumages provide more traits for natural or sexual selection to act upon. Moreover, in upper parts of the bodies, such as the back, the plumage varied more across the different species and evolved faster than in ventral parts, such as the belly or throat. This indicates that sexual selection may be the evolutionary force driving variation in more visible areas, such as the back, while patterns in the ventral part of the body are more important for kin recognition. Eliason et al. further found no differences in plumage complexity between kingfishers located in island or mainland habitats, suggesting that the isolation of the island and the different selection pressures this may bring does not impact the complexity of color patterns. However, kingfisher species located on islands did display higher rates of color evolution. This indicates that, regardless of the complexity of the plumage, island-specific pressures are driving rapid color diversification. Using a new multivariate approach, Eliason et al. have unearthed a pattern in plumage complexity that may otherwise have been missed and, for the first time, have linked differences in color pattern on individual birds with evolutionary differences across species. In doing so, they have provided a framework for future studies of color evolution. The next steps in this research would be to better understand why the island species are evolving more rapidly even though they do not have more complex plumage patterns and how the observed color differences relate to rapid rates of speciation.

Interspecific hybridization explains rapid gorget colour divergence in Heliodoxa hummingbirds (Aves: Trochilidae).

Hybridization is a known source of morphological, functional and communicative signal novelty in many organisms. Although diverse mechanisms of established novel ornamentation have been identified in natural populations, we lack an understanding of hybridization effects across levels of biological scales and upon phylogenies. Hummingbirds display diverse structural colours resulting from coherent light scattering by feather nanostructures. Given the complex relationship between feather nanostructures and the colours they produce, intermediate coloration does not necessarily imply intermediate nanostructures. Here, we characterize nanostructural, ecological and genetic inputs in a distinctive Heliodoxa hummingbird from the foothills of eastern Peru. Genetically, this individual is closely allied with Heliodoxa branickii and Heliodoxa gularis, but it is not identical to either when nuclear data are assessed. Elevated interspecific heterozygosity further suggests it is a hybrid backcross to H. branickii. Electron microscopy and spectrophotometry of this unique individual reveal key nanostructural differences underlying its distinct gorget colour, confirmed by optical modelling. Phylogenetic comparative analysis suggests that the observed gorget coloration divergence from both parentals to this individual would take 6.6-10 My to evolve at the current rate within a single hummingbird lineage. These results emphasize the mosaic nature of hybridization and suggest that hybridization may contribute to the structural colour diversity found across hummingbirds.

Early diversification of avian limb morphology and the role of modularity in the locomotor evolution of crown birds.

High disparity among avian forelimb and hind limb segments in crown birds relative to non-avialan theropod dinosaurs, potentially driven by the origin of separate forelimb and hind limb locomotor modules, has been linked to the evolution of diverse avian locomotor behaviors. However, this hypothesized relationship has rarely been quantitatively investigated in a phylogenetic framework. We assessed the relationship between the evolution of limb morphology and locomotor behavior by comparing a numerical proxy for locomotor disparity to morphospace sizes derived from a dataset of 1,241 extant species. We then estimated how limb disparity accumulated during the crown avian radiation. Lastly, we tested whether limb segments evolved independently between each limb module using phylogenetically informed regressions. Hind limb disparity increased significantly with locomotor disparity after accounting for clade age and species richness. We found that forelimb disparity accumulated rapidly early in avian evolution, whereas hind limb disparity accumulated later, in more recent divergences. We recovered little support for strong correlations between forelimb and hind limb morphology. We posit that these findings support independent evolution of locomotor modules that enabled the striking morphological and behavioral disparity of extant birds.

Wrinkle nanostructures generate a novel form of blue structural color in great argus flight feathers.

Currently known structural colors in feathers are caused by light scattering from periodic or amorphous arrangements of keratin, melanin, and air within barbs and barbules that comprise the feather vane. Structural coloration in the largest part of the feather, the central rachis, is rare. Here, we report on an investigation of the physical mechanisms underlying the only known case of structural coloration in the rachis, the blue rachis of great argus (Argusianus argus) flight feathers. Spectrophotometry revealed a reflectance peak at 344 nm that is diffuse and well matched to the blue and UV-sensitive cone sensitivities of this species' visual system. A combination of electron microscopy and optical modeling confirmed blue coloration is generated by scattering from amorphous wrinkle nanostructures 125 nm deep and 385 nm apart, a new avian coloration mechanism. These findings have implications for understanding how novel courtship phenotypes arise through evolutionary modification of existing ontogenetic templates.

Genomic novelty within a "great speciator" revealed by a high-quality reference genome of the collared kingfisher (Todiramphus chloris collaris).

Islands are natural laboratories for studying patterns and processes of evolution. Research on island endemic birds has revealed elevated speciation rates and rapid phenotypic evolution in several groups (e.g. white-eyes, Darwin's finches). However, understanding the evolutionary processes behind these patterns requires an understanding of how genotypes map to novel phenotypes. To date, there are few high-quality reference genomes for species found on islands. Here, we sequence the genome of one of Ernst Mayr's "great speciators," the collared kingfisher (Todiramphus chloris collaris). Utilizing high molecular weight DNA and linked-read sequencing technology, we assembled a draft high-quality genome with highly contiguous scaffolds (scaffold N50 = 19 Mb). Based on universal single-copy orthologs, we estimated a gene space completeness of 96.6% for the draft genome assembly. The population demographic history analyses reveal a distinct pattern of contraction and expansion in population size throughout the Pleistocene. Comparative genomic analysis of gene family evolution revealed that species-specific and rapidly expanding gene families in the collared kingfisher (relative to other Coraciiformes) are mainly involved in the ErbB signaling pathway and focal adhesion. Todiramphus kingfishers are a species-rich group that has become a focus of speciation research. This draft genome will be a platform for future taxonomic, phylogeographic, and speciation research in the group. For example, target genes will enable testing of changes in sensory structures associated with changes in vision and taste genes across kingfishers.

Evolution of brilliant iridescent feather nanostructures.

The brilliant iridescent plumage of birds creates some of the most stunning color displays known in the natural world. Iridescent plumage colors are produced by nanostructures in feathers and have evolved in diverse birds. The building blocks of these structures-melanosomes (melanin-filled organelles)-come in a variety of forms, yet how these different forms contribute to color production across birds remains unclear. Here, we leverage evolutionary analyses, optical simulations, and reflectance spectrophotometry to uncover general principles that govern the production of brilliant iridescence. We find that a key feature that unites all melanosome forms in brilliant iridescent structures is thin melanin layers. Birds have achieved this in multiple ways: by decreasing the size of the melanosome directly, by hollowing out the interior, or by flattening the melanosome into a platelet. The evolution of thin melanin layers unlocks color-producing possibilities, more than doubling the range of colors that can be produced with a thick melanin layer and simultaneously increasing brightness. We discuss the implications of these findings for the evolution of iridescent structures in birds and propose two evolutionary paths to brilliant iridescence.

Accelerated Brain Shape Evolution Is Associated with Rapid Diversification in an Avian Radiation.

AbstractNiche expansion is a critical step in the speciation process. Large brains linked to improved cognitive ability may enable species to expand their niches and forage in new ways, thereby promoting speciation. Despite considerable work on ecological divergence in brain size and its importance in speciation, relatively little is known about how brain shape relates to behavioral, ecological, and taxonomic diversity at macroevolutionary scales. This is due in part to inherent challenges with quantifying brain shape across many species. Here we present a novel, semiautomated approach for rapidly phenotyping brain shape using semilandmarks derived from X-ray computed microtomography scans. We then test its utility by parsing evolutionary trends within a diverse radiation of birds: kingfishers (Aves: Alcedinidae). Multivariate comparative analyses reveal that rates of brain shape evolution (but not beak shape) are positively correlated with lineage diversification rates. Distinct brain shapes are further associated with changes in body size and foraging behavior, suggesting both allometric and ecological constraints on brain shape evolution. These results are in line with the idea of brains acting as a "master regulator" of critical processes governing speciation, such as dispersal, foraging behavior, and dietary niche.

Cassowary gloss and a novel form of structural color in birds.

One of the two lineages of extant birds resulting from its deepest split, Palaeognathae, has been reported not to exhibit structural coloration in feathers, affecting inferences of ancestral coloration mechanisms in extant birds. Structural coloration in facial skin and eggshells has been shown in this lineage, but has not been reported in feathers. We present the first evidence for two distinct mechanisms of structural color in palaeognath feathers. One extinct volant clade, Lithornithidae, shows evidence of elongate melanin-containing organelles uniquely associated with glossy/iridescent color, a structural color mechanism found in fossil outgroups and neognath birds. We also demonstrate a structural basis for the exceptional gloss in extant cassowary feathers. We propose gloss as an intermediate phenotype between matte and iridescent plumage, conferred by a thick and smooth feather rachis. Rachis-based structural color has not been previously investigated. The new data illuminate the relationships between avian melanin-based coloration and feather structure.

Morphological innovation and biomechanical diversity in plunge-diving birds.

Innovations in foraging behavior can drive morphological diversity by opening up new ways of interacting with the environment, or limit diversity through functional constraints associated with different foraging behaviors. Several classic examples of adaptive radiations in birds show increased variation in ecologically relevant traits. However, these cases primarily focus on geographically narrow adaptive radiations, consider only morphological evolution without a biomechanical approach, or do not investigate tradeoffs with other non-focal traits that might be affected by use of different foraging habitats. Here, we use X-ray microcomputed tomography, biomechanical modeling, and multivariate comparative methods to explore the interplay between foraging behavior and cranial morphology in kingfishers, a global radiation of birds with variable beaks and foraging behaviors, including the archetypal plunge-dive into water. Our results quantify covariation between the shape of the outer keratin covering (rhamphotheca) and the inner skeletal core of the beak, as well as highlight distinct patterns of morphospace occupation for different foraging behaviors and considerable rate variation among these skull regions. We anticipate these findings will have implications for inferring beak shapes in fossil taxa and inform biomimetic design of novel impact-reducing structures.

Signal evolution and morphological complexity in hummingbirds (Aves: Trochilidae).

Understanding how animal signals are produced is critical for understanding their evolution because complexity and modularity in the underlying morphology can affect evolutionary patterns. Hummingbird feathers show some of the brightest and most iridescent colors in nature. These are produced by optically complex stacks of hollow, platelet-shaped organelles called melanosomes. Neither how these morphologies produce colors nor their evolution has been systematically studied. We first used nanoscale morphological measurements and optical modeling to identify the physical basis of color production in 34 hummingbird species. We found that, in general, the melanosome stacks function as multilayer reflectors, with platelet thickness and air space size explaining variation in hue (color) and saturation (color purity). Additionally, light rays reflected from the outer keratin surface interact with those reflected by small, superficial melanosomes to cause secondary reflectance peaks, primarily in short (blue) wavelengths. We then compared variation of both the morphological components and the colors they produce. The outer keratin cortex evolves independently and is more variable than other morphological traits, possibly due to functional constraints on melanosome packing. Intriguingly, shorter wavelength colors evolve faster than longer wavelength colors, perhaps due to developmental processes that enables greater lability of the shapes of small melanosomes. Together, these data indicate that increased structural complexity of feather tissues is associated with greater variation in morphology and iridescent coloration.

Using Historical Biogeography Models to Study Color Pattern Evolution.

Color is among the most striking features of organisms, varying not only in spectral properties like hue and brightness, but also in where and how it is produced on the body. Different combinations of colors on a bird's body are important in both environmental and social contexts. Previous comparative studies have treated plumage patches individually or derived plumage complexity scores from color measurements across a bird's body. However, these approaches do not consider the multivariate nature of plumages (allowing for plumage to evolve as a whole) or account for interpatch distances. Here, we leverage a rich toolkit used in historical biogeography to assess color pattern evolution in a cosmopolitan radiation of birds, kingfishers (Aves: Alcedinidae). We demonstrate the utility of this approach and test hypotheses about the tempo and mode of color evolution in kingfishers. Our results highlight the importance of considering interpatch distances in understanding macroevolutionary trends in color diversity and demonstrate how historical biogeography models are a useful way to model plumage color pattern evolution. Furthermore, they show that distinct color mechanisms (pigments or structural colors) spread across the body in different ways and at different rates. Specifically, net rates are higher for structural colors than pigment-based colors. Together, our study suggests a role for both development and selection in driving extraordinary color pattern diversity in kingfishers. We anticipate this approach will be useful for modeling other complex phenotypes besides color, such as parasite evolution across the body.

How do complex animal signals evolve?

Animal signals-involving combinations of acoustic, chemical, visual, and behavioral cues-are among the most diverse traits in nature. Testing hypotheses about signal evolution has been hampered by difficulties with comparing highly divergent signals among species. In this Primer, I describe recent advances in capturing signals and studying their evolution. I highlight new findings using an information theory-based approach to quantifying signal variation in the diverse birds-of-paradise. Growing access to signal databases in tandem with development of new analytical tools will open up new avenues for studying the proximate mechanisms and ultimate evolutionary causes of signal variation, both within and among species.

Identity and novelty in the avian syrinx.

In its most basic conception, a novelty is simply something new. However, when many previously proposed evolutionary novelties have been illuminated by genetic, developmental, and fossil data, they have refined and narrowed our concept of biological "newness." For example, they show that these novelties can occur at one or multiple levels of biological organization. Here, we review the identity of structures in the avian vocal organ, the syrinx, and bring together developmental data on airway patterning, structural data from across tetrapods, and mathematical modeling to assess what is novel. In contrast with laryngeal cartilages that support vocal folds in other vertebrates, we find no evidence that individual cartilage rings anchoring vocal folds in the syrinx have homology with any specific elements in outgroups. Further, unlike all other vertebrate vocal organs, the syrinx is not derived from a known valve precursor, and its origin involves a transition from an evolutionary "spandrel" in the respiratory tract, the site where the trachea meets the bronchi, to a target for novel selective regimes. We find that the syrinx falls into an unusual category of novel structures: those having significant functional overlap with the structures they replace. The syrinx, along with other evolutionary novelties in sensory and signaling modalities, may more commonly involve structural changes that contribute to or modify an existing function rather than those that enable new functions.

Vocal specialization through tracheal elongation in an extinct Miocene pheasant from China.

Modifications to the upper vocal tract involving hyper-elongated tracheae have evolved many times within crown birds, and their evolution has been linked to a 'size exaggeration' hypothesis in acoustic signaling and communication, whereby smaller-sized birds can produce louder sounds. A fossil skeleton of a new extinct species of wildfowl (Galliformes: Phasianidae) from the late Miocene of China, preserves an elongated, coiled trachea that represents the oldest fossil record of this vocal modification in birds and the first documentation of its evolution within pheasants. The phylogenetic position of this species within Phasianidae has not been fully resolved, but appears to document a separate independent origination of this vocal modification within Galliformes. The fossil preserves a coiled section of the trachea and other remains supporting a tracheal length longer than the bird's body. This extinct species likely produced vocalizations with a lower fundamental frequency and reduced harmonics compared to similarly-sized pheasants. The independent evolution of this vocal feature in galliforms living in both open and closed habitats does not appear to be correlated with other factors of biology or its open savanna-like habitat. Features present in the fossil that are typically associated with sexual dimorphism suggest that sexual selection may have resulted in the evolution of both the morphology and vocalization mechanism in this extinct species.

A bony-crested Jurassic dinosaur with evidence of iridescent plumage highlights complexity in early paravian evolution.

The Jurassic Yanliao theropods have offered rare glimpses of the early paravian evolution and particularly of bird origins, but, with the exception of the bizarre scansoriopterygids, they have shown similar skeletal and integumentary morphologies. Here we report a distinctive new Yanliao theropod species bearing prominent lacrimal crests, bony ornaments previously known from more basal theropods. It shows longer arm and leg feathers than Anchiornis and tail feathers with asymmetrical vanes forming a tail surface area even larger than that in Archaeopteryx. Nanostructures, interpreted as melanosomes, are morphologically similar to organized, platelet-shaped organelles that produce bright iridescent colours in extant birds. The new species indicates the presence of bony ornaments, feather colour and flight-related features consistent with proposed rapid character evolution and significant diversity in signalling and locomotor strategies near bird origins.

Metabolic physiology explains macroevolutionary trends in the melanic colour system across amniotes.

Metabolism links organisms to their environment through its effects on thermoregulation, feeding behaviour and energetics. Genes involved in metabolic processes have known pleiotropic effects on some melanic colour traits. Understanding links between physiology and melanic colour is critical for understanding the role of, and potential constraints on, colour production. Despite considerable variation in metabolic rates and presumed ancestral melanic coloration in vertebrates, few studies have looked at a potential relationship between these two systems in a comparative framework. Here, we test the hypothesis that changes in melanosome shape in integumentary structures track metabolic rate variation across amniotes. Using multivariate comparative analyses and incorporating both extant and fossil taxa, we find significantly faster rates of melanosome shape evolution in taxa with high metabolic rates, as well as both colour- and clade-specific differences in the relationship between metabolic rate and melanosome shape. Phylogenetic tests recover an expansion in melanosome morphospace in maniraptoran dinosaurs, as well as rate shifts within birds (in songbirds) and mammals. These findings indicate another core phenotype influenced by metabolic changes in vertebrates. They also provide a framework for testing clade-specific gene expression patterns in the melanocortin system and may improve colour reconstructions in extinct taxa.

Exceptional preservation and the fossil record of tetrapod integument.

The fossil record of exceptionally preserved soft tissues in Konservat-Lagerstätten provides rare yet significant insight into past behaviours and ecologies. Such deposits are known to occur in bursts rather than evenly through time, but reasons for this pattern and implications for the origins of novel structures remain unclear. Previous assessments of these records focused on marine environments preserving chemically heterogeneous tissues from across animals. Here, we investigate the preservation of skin and keratinous integumentary structures in land-dwelling vertebrates (tetrapods) through time, and in distinct terrestrial and marine depositional environments. We also evaluate previously proposed biotic and abiotic controls on the distribution of 143 tetrapod Konservat-Lagerstätten from the Permian to the Pleistocene in a multivariate framework. Gap analyses taking into account sampling intensity and distribution indicate that feathers probably evolved close to their first appearance in the fossil record. By contrast, hair and archosaur filaments are weakly sampled (five times less common than feathers), and their origins may significantly pre-date earliest known occurrences in the fossil record. This work suggests that among-integument variation in preservation can bias the reconstructed first origins of integumentary novelties and has implications for predicting where, and in what depositional environments, to expect further discoveries of exquisitely preserved tetrapod integument.

Coos, booms, and hoots: The evolution of closed-mouth vocal behavior in birds.

Most birds vocalize with an open beak, but vocalization with a closed beak into an inflating cavity occurs in territorial or courtship displays in disparate species throughout birds. Closed-mouth vocalizations generate resonance conditions that favor low-frequency sounds. By contrast, open-mouth vocalizations cover a wider frequency range. Here we describe closed-mouth vocalizations of birds from functional and morphological perspectives and assess the distribution of closed-mouth vocalizations in birds and related outgroups. Ancestral-state optimizations of body size and vocal behavior indicate that closed-mouth vocalizations are unlikely to be ancestral in birds and have evolved independently at least 16 times within Aves, predominantly in large-bodied lineages. Closed-mouth vocalizations are rare in the small-bodied passerines. In light of these results and body size trends in nonavian dinosaurs, we suggest that the capacity for closed-mouth vocalization was present in at least some extinct nonavian dinosaurs. As in birds, this behavior may have been limited to sexually selected vocal displays, and hence would have co-occurred with open-mouthed vocalizations.