Tip dating and Bayes factors provide insight into the divergences of crown bird clades across the end-Cretaceous mass extinction.

The origin of crown birds (Neornithes) remains contentious owing to conflicting divergence time hypotheses obtained from alternative sources of data. The fossil record suggests limited diversification of Neornithes in the Late Mesozoic and a substantial radiation in the aftermath of the Cretaceous-Palaeogene (K-Pg) mass extinction, approximately 66 Ma. Molecular clock studies, however, have yielded estimates for neornithine origins ranging from the Early Cretaceous (130 Ma) to less than 10 Myr before the K-Pg. We use Bayes factors to compare the fit of node ages from different molecular clock studies to an independent morphological dataset. Our results allow us to reject scenarios of crown bird origins deep in the Early Cretaceous, as well as an origin of crown birds within the last 10 Myr of the Cretaceous. The scenario best supported by our analyses is one where Neornithes originated between the Early and Late Cretaceous (ca 100 Ma), while numerous divergences within major neoavian clades either span or postdate the K-Pg. This study affirms the importance of the K-Pg on the diversification of modern birds, and the potential of combined-evidence tip-dating analyses to illuminate recalcitrant 'rocks versus clocks' debates.

Functional constraints on the number and shape of flight feathers.

As a fundamental ecological aspect of most organisms, locomotor function significantly constrains morphology. At the same time, the evolution of novel locomotor abilities has produced dramatic morphological transformations, initiating some of the most significant diversifications in life history. Despite significant new fossil evidence, it remains unclear whether volant locomotion had a single or multiple origins in pennaraptoran dinosaurs and the volant abilities of individual taxa are controversial. The evolution of powered flight in modern birds involved exaptation of feathered surfaces extending off the limbs and tail yet most studies concerning flight potential in pennaraptorans do not account for the structure and morphology of the wing feathers themselves. Analysis of the number and shape of remex and rectrix feathers across a large dataset of extant birds indicates that the number of remiges and rectrices and the degree of primary vane asymmetry strongly correlate with locomotor ability revealing important functional constraints. Among these traits, phenotypic flexibility varies reflected by the different rates at which morphological changes evolve, such that some traits reflect the ancestral condition, whereas others reflect current locomotor function. While Mesozoic birds and Microraptor have remex morphologies consistent with extant volant birds, that of anchiornithines deviate significantly providing strong evidence this clade was not volant. The results of these analyses support a single origin of dinosaurian flight and indicate the early stages of feathered wing evolution are not sampled by the currently available fossil record.

Macroevolutionary drivers of morphological disparity in the avian quadrate.

In birds, the quadrate connects the mandible and skull, and plays an important role in cranial kinesis. Avian quadrate morphology may therefore be assumed to have been influenced by selective pressures related to feeding ecology, yet large-scale variation in quadrate morphology and its potential relationship with ecology have never been quantitatively investigated. Here, we used geometric morphometrics and phylogenetic comparative methods to quantify morphological variation of the quadrate and its relationship with key ecological features across a wide phylogenetic sample. We found non-significant associations between quadrate shape and feeding ecology across different scales of phylogenetic comparison; indeed, allometry and phylogeny exhibit stronger relationships with quadrate shape than ecological features. We show that similar quadrate shapes are associated with widely varying dietary ecologies (one-to-many mapping), while divergent quadrate shapes are associated with similar dietary ecologies (many-to-one mapping). Moreover, we show that the avian quadrate evolves as an integrated unit and exhibits strong associations with the morphologies of neighbouring bones. Our results collectively illustrate that quadrate shape has evolved jointly with other elements of the avian kinetic system, with the major crown bird lineages exploring alternative quadrate morphologies, highlighting the potential diagnostic value of quadrate morphology in investigations of bird systematics.

A juvenile bird with possible crown-group affinities from a dinosaur-rich Cretaceous ecosystem in North America.

BACKGROUND: Living birds comprise the most speciose and anatomically diverse clade of flying vertebrates, but their poor early fossil record and the lack of resolution around the relationships of the major clades have greatly obscured extant avian origins. RESULTS: Here, I describe a Late Cretaceous bird from North America based on a fragmentary skeleton that includes cranial material and portions of the forelimb, hindlimb, and foot and is identified as a juvenile based on bone surface texture. Several features unite this specimen with crown Aves, but its juvenile status precludes the recognition of a distinct taxon. The North American provenance of the specimen supports a cosmopolitan distribution of early crown birds, clashes with the hypothesized southern hemisphere origins of living birds, and demonstrates that crown birds and their closest relatives coexisted with non-avian dinosaurs that independently converged on avian skeletal anatomy, such as the alvarezsaurids and dromaeosaurids. CONCLUSIONS: By revealing the ecological and biogeographic context of Cretaceous birds within or near the crown clade, the Lance Formation specimen provides new insights into the contingent nature of crown avian survival through the Cretaceous-Paleogene mass extinction and the subsequent origins of living bird diversity.

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.

Limited ecological opportunity influences the tempo of morphological evolution in birds.

According to classic models of lineage diversification and adaptive radiation, phenotypic evolution should accelerate in the context of ecological opportunity and slow down when niches become saturated.1,2 However, only weak support for these ideas has been found in nature, perhaps because most analyses make the biologically unrealistic assumption that clade members contribute equally to reducing ecological opportunity, even when they occur in different continents or specialize on different habitats and diets. To view this problem through a different lens, we adapted a new phylogenetic modeling approach that accounts for the fact that competition for ecological opportunity only occurs between species that coexist and share similar habitats and diets. Applying this method to trait data for nearly all extant species of landbirds,3 we find a widespread signature of decelerating trait evolution in lineages adapted to similar habitats or diets. The strength of this pattern was consistent across latitudes when comparing tropical and temperate assemblages. Our results provide little support for the idea that increased diversity and tighter packing of niches accentuates evolutionary slowdowns in the tropics and instead suggest that limited ecological opportunity can be an important factor determining the rate of morphological diversification at a global scale.

Morphological description of the alimentary canal and adnexal glands in Amazilia tzacatl, Amazilia saucerottei, Amazilia amabilis and Anthrachotorax nigricollis species.

The hummingbird family (Trochilidae) includes the smallest and most metabolically active vertebrates. They have a high energy demand because of their extraordinarily high metabolic rates during hovering while looking for food. The morphology of the digestive apparatus is related to the feeding habits of the species. The anatomy and histology of the digestive apparatus in these birds have not been thoroughly described except for their tongue. Therefore, this study aimed to describe the gross anatomy and histology of the alimentary canal and adnexal glands in four species from the hummingbird family: Amazilia tzacatl (n = 2), Amazilia saucerottei (n = 1), Amazilia amabilis (n = 1) and Anthracothorax nigricollis (n = 1). The alimentary canal was found to be very short. The epithelium of the oesophagus and crop showed variable degrees of keratinization and parakeratotic areas as normal conditions. A dorsal crop was observed as a differential characteristic of these birds. Like other birds, the ventricular mucosa in hummingbirds was covered and protected by the cuticle and showed a tunica muscularis constituted by three muscle layers. There was no isthmus between the proventriculus and ventriculus. The intestine presents a well-differentiated duodenum and jejunum. However, no ileum nor caeca were identified. The intestinal villi length, base width, crypt depth and area showed differences among the specimens studied among the small and large intestines. In addition, variations in thickness were observed in the smooth muscle tunica along the intestine. In all the studied species, the liver was composed of two lobes (right and left), and no gall bladder was observed during gross inspection or in histological sections. Finally, the pancreas was observed as a diffused organ forming islets related to all the small intestines. Some anatomical differences were observed among the studied species, mainly concerning Anthracothorax nigricollis. Hummingbirds showed very interesting and distinctive morphological characteristics. Hummingbirds possess unique and intriguing morphological characteristics. Future comparative studies related to the anatomy, histology and function of the digestive apparatus of hummingbirds are required. Expanding our understanding of the digestive morphophysiology in these bird species is crucial. However, it is necessary to conduct more comprehensive studies encompassing a wider range of hummingbird species and including a larger number of individuals to obtain more conclusive findings.

Reinterpretation of tuberculate cervical vertebrae of Eocene birds as an exceptional anti-predator adaptation against the mammalian craniocervical killing bite.

We report avian cervical vertebrae from the Quercy fissure fillings in France, which are densely covered with villi-like tubercles. Two of these vertebrae stem from a late Eocene site, another lacks exact stratigraphic data. Similar cervical vertebrae occur in avian species from Eocene fossils sites in Germany and the United Kingdom, but the new fossils are the only three-dimensionally preserved vertebrae with pronounced surface sculpturing. So far, the evolutionary significance of this highly bizarre morphology, which is unknown from extant birds, remained elusive, and even a pathological origin was considered. We note the occurrence of similar structures on the skull of the extant African rodent Lophiomys and detail that the tubercles represent true osteological features and characterize a distinctive clade of Eocene birds (Perplexicervicidae). Micro-computed tomography (µCT) shows the tubercles to be associated with osteosclerosis of the cervical vertebrae, which have a very thick cortex and much fewer trabecles and pneumatic spaces than the cervicals of most extant birds aside from some specialized divers. This unusual morphology is likely to have served for strengthening the vertebral spine in the neck region, and we hypothesize that it represents an anti-predator adaptation against the craniocervical killing bite ("neck bite") that evolved in some groups of mammalian predators. Tuberculate vertebrae are only known from the Eocene of Central Europe, which featured a low predation pressure on birds during that geological epoch, as is evidenced by high numbers of flightless avian species. Strengthening of the cranialmost neck vertebrae would have mitigated attacks by smaller predators with weak bite forces, and we interpret these vertebral specializations as the first evidence of "internal bony armor" in birds.

[Protein Repeats Show Clade-Specific Volatility in Aves].

Protein repeats are a source of rapid evolutionary and functional novelty. Repeats are crucial in development, neurogenesis, immunity, and disease. Repeat length variability and purity can alter the outcome of a pathway by altering the protein structure and affecting the protein-protein interaction affinity. Such rampant alterations can facilitate species to rapidly adapt to new environments or acquire various morphological/physiological features. With more than 11000 species, the avian clade is one of the most speciose vertebrate clades, with near-ubiquitous distribution globally. Explosive adaptive radiation and functional diversification facilitated the birds to occupy various habitats. High diversity in morphology, physiology, flight pattern, behavior, coloration, and life histories make birds ideal for studying protein repeats' role in evolutionary novelty. Our results demonstrate a similar repeat diversity and proportion of repeats across all the avian orders considered, implying an essential role of repeats in necessary pathways. We detected positively selected sites (PSS) in the polyQ repeat of RUNX2 in the avian clade; and considerable repeat length contraction in the Psittacopasserae. The repeats show a species-wide bias towards a contraction in Galloanseriformes. Interestingly, we detected the length contrast of polyS repeat in PCDH20 between Galli-formes and Anseriformes. We speculate the length variability of serine repeat and its interaction with ß-catenin in the Wnt/ß-catenin signaling pathway could have facilitated fowls to adapt to their respective environmental conditions. We believe our study emphasizes the role of protein repeats in functional/morphological diversification in birds. We also provide an extensive list of genes with considerable repeat length contrast to further explore the role of length volatility in evolutionary novelty and rapid functional diversification.

Repeated Evolution of Unorthodox Feeding Styles Drives a Negative Correlation between Foot Size and Bill Length in Hummingbirds.

AbstractDifferences among hummingbird species in bill length and shape have rightly been viewed as adaptive in relation to the morphology of the flowers they visit for nectar. In this study we examine functional variation in a behaviorally related but neglected feature: hummingbird feet. We gathered records of hummingbirds clinging by their feet to feed legitimately as pollinators or illegitimately as nectar robbers-"unorthodox" feeding behaviors. We measured key features of bills and feet for 220 species of hummingbirds and compared the 66 known "clinger" species (covering virtually the entire scope of hummingbird body size) with the 144 presumed "non-clinger" species. Once the effects of phylogenetic signal, body size, and elevation above sea level are accounted for statistically, hummingbirds display a surprising but functionally interpretable negative correlation. Clingers with short bills and long hallux (hind-toe) claws have evolved-independently-more than 20 times and in every major clade. Their biomechanically enhanced feet allow them to save energy by clinging to feed legitimately on short-corolla flowers and by stealing nectar from long-corolla flowers. In contrast, long-billed species have shorter hallux claws, as plant species with long-corolla flowers enforce hovering to feed, simply by the way they present their flowers.

The Comparative Anatomy of the Upper Digestive System in 26 Species of Zoophagous-Polyphagous Palearctic Birds / Anatomía Comparada del Sistema Digestivo Superior en 26 Especies de Aves Paleárticas Zoófagas-Polífagas

SUMMARY: Birds are the most diversified organisms on Earth, with species covering various niches in each major biome, being essential to understand the modern ecosystem. This study concentrates on the diversification of the anatomical structure of the upper digestive tract for 26 species of zoophage-polyphagous birds and the anatomical differences in the digestive system to reveal aspects related to their evolution and diversification. The trophic spectrum of the selected birds includes several categories of food, or, as in the case of strictly carnivorous birds, to a single food category. After performing the dissections, the digestive tract was separated from the carcass and each digestive segment was measured and analysed. In this study, it was demonstrated that the birds' feeding behaviour influence the macroscopic particularities of the digestive system, more visible in the cranial portion (oropharyngeal cavity, esophagus, proventriculus and gizzard), with little descriptive information in the literature. The tongue is poorly developed and immobile in piscivorous birds, while the tongue of insectivorous birds is long and moves considerably away from the tip of the bill. The esophagus was stretchable and presents longitudinal folds on its entire surface in piscivorous species and not extensible in insectivorous birds.

Las aves son los organismos más diversificados de la Tierra, con especies que cubren varios nichos en cada bioma principal, siendo esenciales para comprender el ecosistema moderno. Este estudio se concentra en la diversificación de la estructura anatómica del tracto digestivo superior para 26 especies de aves zoófago-polífagas y las diferencias anatómicas en el sistema digestivo para revelar aspectos relacionados con su evolución y diversificación. El espectro trófico de las aves seleccionadas incluye varias categorías de alimentos o, como en el caso de las aves estrictamente carnívoras, una sola categoría de alimentos. Después de realizar las disecciones, se separó el tracto digestivo de la canal y se midió y analizó cada segmento digestivo. En este estudio se demostró que el comportamiento alimentario de las aves influye en las particularidades macroscópicas del sistema digestivo, más visibles en la porción craneal (cavidad orofaríngea, esófago, proventrículo y molleja), con poca información descriptiva en la literatura. En las aves piscívoras, la lengua está poco desarrollada e inmóvil, mientras que la lengua de las aves insectívoras es larga y se aleja considerablemente de la punta del pico. El esófago era estirable y presentaba pliegues longitudinales en toda su superficie en especies piscívoras y no extensible en aves insectívoras.

A new avialan theropod from an emerging Jurassic terrestrial fauna.

Birds are descended from non-avialan theropod dinosaurs of the Late Jurassic period, but the earliest phase of this evolutionary process remains unclear owing to the exceedingly sparse and spatio-temporally restricted fossil record1-5. Information about the early-diverging species along the avialan line is crucial to understand the evolution of the characteristic bird bauplan, and to reconcile phylogenetic controversies over the origin of birds3,4. Here we describe one of the stratigraphically youngest and geographically southernmost Jurassic avialans, Fujianvenator prodigiosus gen. et sp. nov., from the Tithonian age of China. This specimen exhibits an unusual set of morphological features that are shared with other stem avialans, troodontids and dromaeosaurids, showing the effects of evolutionary mosaicism in deep avialan phylogeny. F. prodigiosus is distinct from all other Mesozoic avialan and non-avialan theropods in having a particularly elongated hindlimb, suggestive of a terrestrial or wading lifestyle-in contrast with other early avialans, which exhibit morphological adaptations to arboreal or aerial environments. During our fieldwork in Zhenghe where F. prodigiosus was found, we discovered a diverse assemblage of vertebrates dominated by aquatic and semi-aquatic species, including teleosts, testudines and choristoderes. Using in situ radioisotopic dating and stratigraphic surveys, we were able to date the fossil-containing horizons in this locality-which we name the Zhenghe Fauna-to 148-150 million years ago. The diversity of the Zhenghe Fauna and its precise chronological framework will provide key insights into terrestrial ecosystems of the Late Jurassic.

Digest: Ecological and life-history drivers of avian skull evolution.

What are the factors that drive the patterns and evolutionary rates of morphological characteristics? To answer this question, Hunt et al. explore shape variation and rates of change in modern avian skulls using morphometric measurements and phylogenetic analyses. They find that habitat density and migration have the strongest influences on avian skull variation and that denser habitats, longer migratory distances, and precocial developmental modes are all associated with faster rates of morphological evolution.

Online repositories of photographs and videos provide insights into the evolution of skilled hindlimb movements in birds.

The ability to manipulate objects with limbs has evolved repeatedly among land tetrapods. Several selective forces have been proposed to explain the emergence of forelimb manipulation, however, work has been largely restricted to mammals, which prevents the testing of evolutionary hypotheses in a comprehensive evolutionary framework. In birds, forelimbs have gained the exclusive function of flight, with grasping transferred predominantly to the beak. In some birds, the feet are also used in manipulative tasks and appear to share some features with manual grasping and prehension in mammals, but this has not been systematically investigated. Here we use large online repositories of photographs and videos to quantify foot manipulative skills across a large sample of bird species (>1000 species). Our results show that a complex interaction between niche, diet and phylogeny drive the evolution of manipulative skills with the feet in birds. Furthermore, we provide strong support for the proposition that an arboreal niche is a key element in the evolution of manipulation in land vertebrates. Our systematic comparison of foot use in birds provides a solid base for understanding morphological and neural adaptations for foot use in birds, and for studying the convergent evolution of manipulative skills in birds and mammals.

Low morphological disparity and decelerated rate of limb size evolution close to the origin of birds.

The origin of birds from theropod dinosaurs involves many changes in musculoskeletal anatomy and epidermal structures, including multiple instances of convergence and homology-related traits that contribute to the refinement of flight capability. Changes in limb sizes and proportions are important for locomotion (for example, the forelimb for bird flight); thus, understanding these patterns is central to investigating the transition from terrestrial to volant theropods. Here we analyse the patterns of morphological disparity and the evolutionary rate of appendicular limbs along avialan stem lineages using phylogenetic comparative approaches. Contrary to the traditional wisdom that an evolutionary innovation like flight would promote and accelerate evolvability, our results show a shift to low disparity and decelerated rate near the origin of avialans that is largely ascribed to the evolutionarily constrained forelimb. These results suggest that natural selection shaped patterns of limb evolution close to the origin of avialans in a way that may reflect the winged forelimb 'blueprint' associated with powered flight.

Plant-hummingbird pollination networks exhibit limited rewiring after experimental removal of a locally abundant plant species.

Mutualistic relationships, such as those between plants and pollinators, may be vulnerable to the local extinctions predicted under global environmental change. However, network theory predicts that plant-pollinator networks can withstand species loss if pollinators switch to alternative floral resources (rewiring). Whether rewiring occurs following species loss in natural communities is poorly known because replicated species exclusions are difficult to implement at appropriate spatial scales. We experimentally removed a hummingbird-pollinated plant, Heliconia tortuosa, from within tropical forest fragments to investigate how hummingbirds respond to temporary loss of an abundant resource. Under the rewiring hypothesis, we expected that behavioural flexibility would allow hummingbirds to use alternative resources, leading to decreased ecological specialization and reorganization of the network structure (i.e. pairwise interactions). Alternatively, morphological or behavioural constraints-such as trait-matching or interspecific competition-might limit the extent to which hummingbirds alter their foraging behaviour. We employed a replicated Before-After-Control-Impact experimental design and quantified plant-hummingbird interactions using two parallel sampling methods: pollen collected from individual hummingbirds ('pollen networks', created from >300 pollen samples) and observations of hummingbirds visiting focal plants ('camera networks', created from >19,000 observation hours). To assess the extent of rewiring, we quantified ecological specialization at the individual, species and network levels and examined interaction turnover (i.e. gain/loss of pairwise interactions). H. tortuosa removal caused some reorganization of pairwise interactions but did not prompt large changes in specialization, despite the large magnitude of our manipulation (on average, >100 inflorescences removed in exclusion areas of >1 ha). Although some individual hummingbirds sampled through time showed modest increases in niche breadth following Heliconia removal (relative to birds that did not experience resource loss), these changes were not reflected in species- and network-level specialization metrics. Our results suggest that, at least over short time-scales, animals may not necessarily shift to alternative resources after losing an abundant food resource-even in species thought to be highly opportunistic foragers, such as hummingbirds. Given that rewiring contributes to theoretical predictions of network stability, future studies should investigate why pollinators might not expand their diets after a local resource extinction.

New Data on Hesperornithids (Aves: Ornithurae) from the Campanian of the Lower Volga Region (Late Cretaceous, Russia).

Taxonomic diversity of Late Cretaceous hesperornithids (Aves: Hesperornithidae) of European Russia and Eastern Europe as a whole remain poorly understood, and the morphology of these large flightless birds is poorly known. New finds of Hesperornithidae in the Karyakino locality (Saratov oblast, Russia) confirm the coexistence of two forms of these flightless seabirds in the Campanian (mid-Late Cretaceous) of the Lower Volga region. A femur is described for the first time for Hesperornis rossicus Nessov et Yarkov, 1993, indicating that this large species is morphologically distinct from North American H. regalis Marsh, 1872.

Incipient wing flapping enhances aerial performance of a robotic paravian model.

The functional origins of bird flight remain unresolved despite a diversity of hypothesized selective factors. Fossil taxa phylogenetically intermediate between typical theropod dinosaurs and modern birds exhibit dense aggregations of feathers on their forelimbs, and the evolving morphologies and kinematic activational patterns of these structures could have progressively enhanced aerodynamic force production over time. However, biomechanical functionality of flapping in such transitional structures is unknown. We evaluated a robot inspired by paravian morphology to model the effects of incremental increases in wing length, wingbeat frequency, and stroke amplitude on aerial performance. From a launch height of 2.8 m, wing elongation most strongly influenced distance travelled and time aloft for all frequency-amplitude combinations, although increased frequency and amplitude also enhanced performance. Furthermore, we found interaction effects among these three parameters such that when the wings were long, higher values of either wingbeat frequency or stroke amplitude synergistically improved performance. For launches from a height of 5.0 m, the effects of these flapping parameters appear to diminish such that only flapping at the highest frequency (5.7 Hz) and amplitude (60°) significantly increased performance. Our results suggest that a gliding animal at the physical scale relevant to bird flight origins, and with transitional wings, can improve aerodynamic performance via rudimentary wing flapping at relatively low frequencies and amplitudes. Such gains in horizontal translation and time aloft, as those found in this study, are likely to be advantageous for any taxon that engages in aerial behavior for purposes of transit or escape. This study thus demonstrates aerodynamic benefits of transition from a gliding stage to full-scale wing flapping in paravian taxa.

Morphology and niche evolution influence hummingbird speciation rates.

How traits affect speciation is a long-standing question in evolution. We investigate whether speciation rates are affected by the traits themselves or by the rates of their evolution, in hummingbirds, a clade with great variation in speciation rates, morphology and ecological niches. Further, we test two opposing hypotheses, postulating that speciation rates are promoted by trait conservatism or, alternatively, by trait divergence. To address these questions, we analyse morphological (body mass and bill length) and niche traits (temperature and precipitation position and breadth, and mid-elevation), using a variety of methods to estimate speciation rates and correlate them with traits and their evolutionary rates. When it comes to the traits, we find faster speciation in smaller hummingbirds with shorter bills, living at higher elevations and experiencing greater temperature ranges. As for the trait evolutionary rates, we find that speciation increases with rates of divergence in the niche traits, but not in the morphological traits. Together, these results reveal the interplay of mechanisms through which different traits and their evolutionary rates (conservatism or divergence) influence the origination of hummingbird diversity.