Corrigendum: Mega-evolutionary dynamics of the adaptive radiation of birds.

This corrects the article DOI: 10.1038/nature21074.

Mega-evolutionary dynamics of the adaptive radiation of birds.

The origin and expansion of biological diversity is regulated by both developmental trajectories and limits on available ecological niches. As lineages diversify, an early and often rapid phase of species and trait proliferation gives way to evolutionary slow-downs as new species pack into ever more densely occupied regions of ecological niche space. Small clades such as Darwin's finches demonstrate that natural selection is the driving force of adaptive radiations, but how microevolutionary processes scale up to shape the expansion of phenotypic diversity over much longer evolutionary timescales is unclear. Here we address this problem on a global scale by analysing a crowdsourced dataset of three-dimensional scanned bill morphology from more than 2,000 species. We find that bill diversity expanded early in extant avian evolutionary history, before transitioning to a phase dominated by packing of morphological space. However, this early phenotypic diversification is decoupled from temporal variation in evolutionary rate: rates of bill evolution vary among lineages but are comparatively stable through time. We find that rare, but major, discontinuities in phenotype emerge from rapid increases in rate along single branches, sometimes leading to depauperate clades with unusual bill morphologies. Despite these jumps between groups, the major axes of within-group bill-shape evolution are remarkably consistent across birds. We reveal that macroevolutionary processes underlying global-scale adaptive radiations support Darwinian and Simpsonian ideas of microevolution within adaptive zones and accelerated evolution between distinct adaptive peaks.

Diet of Mesozoic toothed birds (Longipterygidae) inferred from quantitative analysis of extant avian diet proxies.

BACKGROUND: Birds are key indicator species in extant ecosystems, and thus we would expect extinct birds to provide insights into the nature of ancient ecosystems. However, many aspects of extinct bird ecology, particularly their diet, remain obscure. One group of particular interest is the bizarre toothed and long-snouted longipterygid birds. Longipterygidae is the most well-understood family of enantiornithine birds, the dominant birds of the Cretaceous period. However, as with most Mesozoic birds, their diet remains entirely speculative. RESULTS: To improve our understanding of longipterygids, we investigated four proxies in extant birds to determine diagnostic traits for birds with a given diet: body mass, claw morphometrics, jaw mechanical advantage, and jaw strength via finite element analysis. Body mass of birds tended to correspond to the size of their main food source, with both carnivores and herbivores splitting into two subsets by mass: invertivores or vertivores for carnivores, and granivores + nectarivores or folivores + frugivores for herbivores. Using claw morphometrics, we successfully distinguished ground birds, non-raptorial perching birds, and raptorial birds from one another. We were unable to replicate past results isolating subtypes of raptorial behaviour. Mechanical advantage was able to distinguish herbivorous diets with particularly high values of functional indices, and so is useful for identifying these specific diets in fossil taxa, but overall did a poor job of reflecting diet. Finite element analysis effectively separated birds with hard and/or tough diets from those eating foods which are neither, though could not distinguish hard and tough diets from one another. We reconstructed each of these proxies in longipterygids as well, and after synthesising the four lines of evidence, we find all members of the family but Shengjingornis (whose diet remains inconclusive) most likely to be invertivores or generalist feeders, with raptorial behaviour likely in Longipteryx and Rapaxavis. CONCLUSIONS: This study provides a 20% increase in quantitatively supported fossil bird diets, triples the number of diets reconstructed in enantiornithine species, and serves as an important first step in quantitatively investigating the origins of the trophic diversity of living birds. These findings are consistent with past hypotheses that Mesozoic birds occupied low trophic levels.

Global biogeographic patterns of avian morphological diversity.

Understanding the biogeographical patterns, and evolutionary and environmental drivers, underpinning morphological diversity are key for determining its origins and conservation. Using a comprehensive set of continuous morphological traits extracted from museum collections of 8353 bird species, including geometric morphometric beak shape data, we find that avian morphological diversity is unevenly distributed globally, even after controlling for species richness, with exceptionally dense packing of species in hyper-diverse tropical hotspots. At the regional level, these areas also have high morphological variance, with species exhibiting high phenotypic diversity. Evolutionary history likely plays a key role in shaping these patterns, with evolutionarily old species contributing to niche expansion, and young species contributing to niche packing. Taken together, these results imply that the tropics are both 'cradles' and 'museums' of phenotypic diversity.

Craniofacial development illuminates the evolution of nightbirds (Strisores).

Evolutionary variation in ontogeny played a central role in the origin of the avian skull. However, its influence in subsequent bird evolution is largely unexplored. We assess the links between ontogenetic and evolutionary variation of skull morphology in Strisores (nightbirds). Nightbirds span an exceptional range of ecologies, sizes, life-history traits and craniofacial morphologies constituting an ideal test for evo-devo hypotheses of avian craniofacial evolution. These morphologies include superficially 'juvenile-like' broad, flat skulls with short rostra and large orbits in swifts, nightjars and allied lineages, and the elongate, narrow rostra and globular skulls of hummingbirds. Here, we show that nightbird skulls undergo large ontogenetic shape changes that differ strongly from widespread avian patterns. While the superficially juvenile-like skull morphology of many adult nightbirds results from convergent evolution, rather than paedomorphosis, the divergent cranial morphology of hummingbirds originates from an evolutionary reversal to a more typical avian ontogenetic trajectory combined with accelerated ontogenetic shape change. Our findings underscore the evolutionary lability of cranial growth and development in birds, and the underappreciated role of this aspect of phenotypic variability in the macroevolutionary diversification of the amniote skull.

The multifactorial nature of beak and skull shape evolution in parrots and cockatoos (Psittaciformes).

BACKGROUND: The Psittaciformes (parrots and cockatoos) are characterised by their large beaks, and are renowned for their ability to produce high bite forces. These birds also possess a suite of modifications to their cranial architecture interpreted to be adaptations for feeding on mechanically resistant foods, yet the relationship between cranial morphology and diet has never been explicitly tested. Here, we provide a three-dimensional geometric morphometric analysis of the developmental and biomechanical factors that may be influencing the evolution of psittaciformes' distinctive cranial morphologies. RESULTS: Contrary to our own predictions, we find that dietary preferences for more- or less- mechanically resistant foods have very little influence on beak and skull shape, and that diet predicts only 2.4% of the shape variation in psittaciform beaks and skulls. Conversely, evolutionary allometry and integration together predict almost half the observed shape variation, with phylogeny remaining an important factor in shape identity throughout our analyses, particularly in separating cockatoos (Cacatuoidea) from the true parrots (Psittacoidea). CONCLUSIONS: Our results are similar to recent findings about the evolutionary trajectories of skull and beak shape in other avian families. We therefore propose that allometry and integration are important factors causing canalization of the avian head, and while diet clearly has an influence on beak shape between families, this may not be as important at driving evolvability within families as is commonly assumed.

The shapes of bird beaks are highly controlled by nondietary factors.

Bird beaks are textbook examples of ecological adaptation to diet, but their shapes are also controlled by genetic and developmental histories. To test the effects of these factors on the avian craniofacial skeleton, we conducted morphometric analyses on raptors, a polyphyletic group at the base of the landbird radiation. Despite common perception, we find that the beak is not an independently targeted module for selection. Instead, the beak and skull are highly integrated structures strongly regulated by size, with axes of shape change linked to the actions of recently identified regulatory genes. Together, size and integration account for almost 80% of the shape variation seen between different species to the exclusion of morphological dietary adaptation. Instead, birds of prey use size as a mechanism to modify their feeding ecology. The extent to which shape variation is confined to a few major axes may provide an advantage in that it facilitates rapid morphological evolution via changes in body size, but may also make raptors especially vulnerable when selection pressures act against these axes. The phylogenetic position of raptors suggests that this constraint is prevalent in all landbirds and that breaking the developmental correspondence between beak and braincase may be the key novelty in classic passerine adaptive radiations.

Open data and digital morphology.

Over the past two decades, the development of methods for visualizing and analysing specimens digitally, in three and even four dimensions, has transformed the study of living and fossil organisms. However, the initial promise that the widespread application of such methods would facilitate access to the underlying digital data has not been fully achieved. The underlying datasets for many published studies are not readily or freely available, introducing a barrier to verification and reproducibility, and the reuse of data. There is no current agreement or policy on the amount and type of data that should be made available alongside studies that use, and in some cases are wholly reliant on, digital morphology. Here, we propose a set of recommendations for minimum standards and additional best practice for three-dimensional digital data publication, and review the issues around data storage, management and accessibility.

Digital dissection - using contrast-enhanced computed tomography scanning to elucidate hard- and soft-tissue anatomy in the Common Buzzard Buteo buteo.

Gross dissection has a long history as a tool for the study of human or animal soft- and hard-tissue anatomy. However, apart from being a time-consuming and invasive method, dissection is often unsuitable for very small specimens and often cannot capture spatial relationships of the individual soft-tissue structures. The handful of comprehensive studies on avian anatomy using traditional dissection techniques focus nearly exclusively on domestic birds, whereas raptorial birds, and in particular their cranial soft tissues, are essentially absent from the literature. Here, we digitally dissect, identify, and document the soft-tissue anatomy of the Common Buzzard (Buteo buteo) in detail, using the new approach of contrast-enhanced computed tomography using Lugol's iodine. The architecture of different muscle systems (adductor, depressor, ocular, hyoid, neck musculature), neurovascular, and other soft-tissue structures is three-dimensionally visualised and described in unprecedented detail. The three-dimensional model is further presented as an interactive PDF to facilitate the dissemination and accessibility of anatomical data. Due to the digital nature of the data derived from the computed tomography scanning and segmentation processes, these methods hold the potential for further computational analyses beyond descriptive and illustrative proposes.

Synthetic analysis of trophic diversity and evolution in Enantiornithes with new insights from Bohaiornithidae.

Enantiornithines were the dominant birds of the Mesozoic, but understanding of their diet is still tenuous. We introduce new data on the enantiornithine family Bohaiornithidae, famous for their large size and powerfully built teeth and claws. In tandem with previously published data, we comment on the breadth of enantiornithine ecology and potential patterns in which it evolved. Body mass, jaw mechanical advantage, finite element analysis of the jaw, and traditional morphometrics of the claws and skull are compared between bohaiornithids and living birds. We find bohaiornithids to be more ecologically diverse than any other enantiornithine family: Bohaiornis and Parabohaiornis are similar to living plant-eating birds; Longusunguis resembles raptorial carnivores; Zhouornis is similar to both fruit-eating birds and generalist feeders; and Shenqiornis and Sulcavis plausibly ate fish, plants, or a mix of both. We predict the ancestral enantiornithine bird to have been a generalist which ate a wide variety of foods. However, more quantitative data from across the enantiornithine tree is needed to refine this prediction. By the Early Cretaceous, enantiornithine birds had diversified into a variety of ecological niches like crown birds after the K-Pg extinction, adding to the evidence that traits unique to crown birds cannot completely explain their ecological success.

The birds living in the world today are only a small part of the larger bird family tree. Around 120 to 65 million years ago, when dinosaurs and other large reptiles roamed the world, the ancestors of modern-day birds were actually rather rare. Instead, another now extinct group of birds called the Enantiornithes (meaning "opposite birds") were the most common birds. Many researchers believe that Enantiornithes may have filled similar roles in ancient ecosystems as living birds do today. For example, some may have hunted other birds or animals, while some may have eaten only plants. Some may have specialized at eating a few specific foods while others may have been 'generalists' that ate many different foods. However, some of the physical features of Enantiornithes set them apart from modern-day birds. For example, unlike living birds, Enantiornithes had teeth and their wings were also constructed very differently. Previous studies suggest that one group of these extinct birds most likely ate insects and another group most likely ate fish, but it remains unclear what variety of foods opposite birds as a whole may have consumed. Miller et al. compared the jaws, claws and various other physical features of fossils from six additional species of opposite birds with the skeletons of modern birds to infer what the diets of these opposite birds may have been. This approach revealed that Enantiornithes may have had a wide variety of different diets. The researchers found that two species probably ate plants, another species most likely ate meat, and another one likely ate a mixture of both. With a large sample across Enantiornithes, Miller et al. were able to predict the diet of their common ancestor. They found the common ancestor to most likely be a 'generalist' eating variety of foods and that some species subsequently evolved to have more specialist diets. Opposite birds probably played many different roles in ecosystems, like living birds do today. Therefore, a better understanding how Enantiornithes evolved may shed light on the factors that have influenced the evolution of modern-day birds. This may aid future conservation efforts to target birds whose descendants may be able to take up the ecological roles of other species that go extinct.

Quantitative investigation of pengornithid enantiornithine diet reveals macrocarnivorous ecology evolved in birds by Early Cretaceous.

The diet of Mesozoic birds is poorly known, limiting evolutionary understanding of birds' roles in modern ecosystems. Pengornithidae is one of the best understood families of Mesozoic birds, hypothesized to eat insects or only small amounts of meat. We investigate these hypotheses with four lines of evidence: estimated body mass, claw traditional morphometrics, jaw mechanical advantage, and jaw finite element analysis. Owing to limited data, the diets of Eopengornis and Chiappeavis remain obscure. Pengornis, Parapengornis, and Yuanchuavis show adaptations for vertebrate carnivory. Pengornis also has talons similar to living raptorial birds like caracaras that capture and kill large prey, which represents the earliest known adaptation for macrocarnivory in a bird. This supports the appearance of this ecology ∼35 million years earlier than previously thought. These findings greatly increase the niche breadth known for Early Cretaceous birds, and shift the prevailing view that Mesozoic birds mainly occupied low trophic levels.

Three-dimensional visualization of predatory gastropod feeding teeth with synchrotron scanning.

Several families of neogastropod mollusks independently evolved the ability to drill through mineralized prey skeletons using their own mineralized feeding teeth, sometimes with shell-softening chemical agents produced by an organ in the foot. Teeth with more durable tooth shapes should extend their use and improve predator performance, but past studies have described only the cusped-side of teeth, mostly overlooking morphologies related to functional interactions between teeth. Here, we describe the three-dimensional morphology of the central drilling tooth (rachidian) from four species of the neogastropod family Muricidae using synchrotron tomographic microscopy and assemble a three-dimensional model of a multitooth series in drilling position for two of them to investigate their dynamic form. We find two new types of articulating surfaces, including a saddle joint at either end of the rachidian and a large tongue-and-groove joint in the center. The latter has a shape that maximizes contact surface area between teeth as they rotate away from each other during drilling. Articulating joints have not been described in Neogastropod radula previously, but they are consistent with an earlier hypothesis that impact forces on individual teeth during predatory drilling are dispersed by tooth-tooth interactions.

Innovation and elaboration on the avian tree of life.

Widely documented, megaevolutionary jumps in phenotypic diversity continue to perplex researchers because it remains unclear whether these marked changes can emerge from microevolutionary processes. Here, we tackle this question using new approaches for modeling multivariate traits to evaluate the magnitude and distribution of elaboration and innovation in the evolution of bird beaks. We find that elaboration, evolution along the major axis of phenotypic change, is common at both macro- and megaevolutionary scales, whereas innovation, evolution away from the major axis of phenotypic change, is more prominent at megaevolutionary scales. The major axis of phenotypic change among species beak shapes at megaevolutionary scales is an emergent property of innovation across clades. Our analyses suggest that the reorientation of phenotypes via innovation is a ubiquitous route for divergence that can arise through gradual change alone, opening up further avenues for evolution to explore.

Is shape in the eye of the beholder? Assessing landmarking error in geometric morphometric analyses on live fish.

Geometric morphometrics is widely used to quantify morphological variation between biological specimens, but the fundamental influence of operator bias on data reproducibility is rarely considered, particularly in studies using photographs of live animals taken under field conditions. We examined this using four independent operators that applied an identical landmarking scheme to replicate photographs of 291 live Atlantic salmon (Salmo salar L.) from two rivers. Using repeated measures tests, we found significant inter-operator differences in mean body shape, suggesting that the operators introduced a systematic error despite following the same landmarking scheme. No significant differences were detected when the landmarking process was repeated by the same operator on a random subset of photographs. Importantly, in spite of significant operator bias, small but statistically significant morphological differences between fish from the two rivers were found consistently by all operators. Pairwise tests of angles of vectors of shape change showed that these between-river differences in body shape were analogous across operator datasets, suggesting a general reproducibility of findings obtained by geometric morphometric studies. In contrast, merging landmark data when fish from each river are digitised by different operators had a significant impact on downstream analyses, highlighting an intrinsic risk of bias. Overall, we show that, even when significant inter-operator error is introduced during digitisation, following an identical landmarking scheme can identify morphological differences between populations. This study indicates that operators digitising at least a sub-set of all data groups of interest may be an effective way of mitigating inter-operator error and potentially enabling data sharing.

Models in palaeontological functional analysis.

Models are a principal tool of modern science. By definition, and in practice, models are not literal representations of reality but provide simplifications or substitutes of the events, scenarios or behaviours that are being studied or predicted. All models make assumptions, and palaeontological models in particular require additional assumptions to study unobservable events in deep time. In the case of functional analysis, the degree of missing data associated with reconstructing musculoskeletal anatomy and neuronal control in extinct organisms has, in the eyes of some scientists, rendered detailed functional analysis of fossils intractable. Such a prognosis may indeed be realized if palaeontologists attempt to recreate elaborate biomechanical models based on missing data and loosely justified assumptions. Yet multiple enabling methodologies and techniques now exist: tools for bracketing boundaries of reality; more rigorous consideration of soft tissues and missing data and methods drawing on physical principles that all organisms must adhere to. As with many aspects of science, the utility of such biomechanical models depends on the questions they seek to address, and the accuracy and validity of the models themselves.

Sensitivity and ex vivo validation of finite element models of the domestic pig cranium.

A finite element (FE) validation and sensitivity study was undertaken on a modern domestic pig cranium. Bone strain data were collected ex vivo from strain gauges, and compared with results from specimen-specific FE models. An isotropic, homogeneous model was created, then input parameters were altered to investigate model sensitivity. Heterogeneous, isotropic models investigated the effects of a constant-thickness, stiffer outer layer (representing cortical bone) atop a more compliant interior (representing cancellous bone). Loading direction and placement of strain gauges were also varied, and the use of 2D membrane elements at strain gauge locations as a method of projecting 3D model strains into the plane of the gauge was investigated. The models correctly estimate the loading conditions of the experiment, yet at some locations fail to reproduce correct principal strain magnitudes, and hence strain ratios. Principal strain orientations are predicted well. The initial model was too stiff by approximately an order of magnitude. Introducing a compliant interior reported strain magnitudes more similar to the ex vivo results without notably affecting strain orientations, ratios or contour patterns, suggesting that this simple heterogeneity was the equivalent of reducing the overall stiffness of the model. Models were generally insensitive to moderate changes in loading direction or strain gauge placement, except in the squamosal portion of the zygomatic arch. The use of membrane elements made negligible differences to the reported strains. The models therefore seem most sensitive to changes in material properties, and suggest that failure to model local heterogeneity in material properties and structure of the bone may be responsible for discrepancies between the experimental and model results. This is partially attributable to a lack of resolution in the CT scans from which the model was built, and partially due to an absence of detailed material properties data for pig cranial bone. Thus, caution is advised when using FE models to estimate absolute numerical values of breaking stress and bite force unless detailed input parameters are available. However, if the objective is to compare relative differences between models, the fact that the strain environment is replicated well means that such investigations can be robust.

The consequences of craniofacial integration for the adaptive radiations of Darwin's finches and Hawaiian honeycreepers.

The diversifications of Darwin's finches and Hawaiian honeycreepers are two text-book examples of adaptive radiation in birds. Why these two bird groups radiated while the remaining endemic birds in these two archipelagos exhibit relatively low diversity and disparity remains unexplained. Ecological factors have failed to provide a convincing answer to this phenomenon, and some intrinsic causes connected to craniofacial evolution have been hypothesized. The tight coevolution of the beak and the remainder of the skull in diurnal raptors and parrots suggests that integration may be the prevalent condition in landbirds (Inopinaves). This is in contrast with the archetypal relationship between beak shape and ecology in Darwin's finches and Hawaiian honeycreepers, which suggests that the beak can adapt as a distinct module in these birds. Modularity has therefore been proposed to underpin the adaptive radiation of these groups, allowing the beak to evolve more rapidly and freely in response to ecological opportunity. Here, using geometric morphometrics and phylogenetic comparative methods in a broad sample of landbird skulls, we show that craniofacial evolution in Darwin's finches and Hawaiian honeycreepers seems to be characterized by a tighter coevolution of the beak and the rest of the skull (cranial integration) than in most landbird lineages, with rapid and extreme morphological evolution of both skull regions along constrained directions of phenotypic space. These patterns are unique among landbirds, including other sympatric island radiations, and therefore counter previous hypotheses by showing that tighter cranial integration, not only modularity, can facilitate evolution along adaptive directions.

Disassociated rhamphotheca of fossil bird Confuciusornis informs early beak reconstruction, stress regime, and developmental patterns.

Soft tissue preservation in fossil birds provides a rare window into their anatomy, function, and development. Here, we present an exceptionally-preserved specimen of Confuciusornis which, through Laser-Stimulated Fluorescence imaging, is identified as preserving a disassociated rhamphotheca. Reconstruction of the in vivo position of the rhamphotheca validates the association of the rhamphotheca with two previous confuciusornithid specimens while calling that of a third specimen into question. The ease of dissociation is discussed and proposed with a fourth specimen alongside finite element analysis as evidence for preferential soft-food feeding. However, this proposition remains tentative until there is a better understanding of the functional role of beak attachment in living birds. Differences in post-rostral extent and possibly rhamphotheca curvature between confuciusornithids and modern birds hint at developmental differences between the two. Together, this information provides a wealth of new information regarding the nature of the beak outside crown Aves.

The evolutionary relationship among beak shape, mechanical advantage, and feeding ecology in modern birds.

Extensive research on avian adaptive radiations has led to a presumption that beak morphology predicts feeding ecology in birds. However, this ecomorphological relationship has only been quantified in a handful of avian lineages, where associations are of variable strength, and never at a broad macroevolutionary scale. Here, we used shape analysis and phylogenetic comparative methods to quantify the relationships among beak shape, mechanical advantage, and two measures of feeding ecology (feeding behavior and semiquantitative dietary preferences) in a broad sample of modern birds, comprising most living orders. We found a complex relationship, with most variables showing a significant relationship with feeding ecology but little explanatory power. For example, diet accounts for less than 12% of beak shape variation. Similar beak shapes are associated with disparate dietary regimes, even when accounting for diet-feeding behavior relationships and phylogeny. Very few lineages optimize for stronger bite forces, with most birds exhibiting relatively fast, weak bites, even in large predatory taxa. The extreme morphological and behavioral flexibility of the beak in birds suggests that, far from being an exemplary feeding adaptation, avian beak diversification may have been largely contingent on trade-offs and constraints.

Scaling and functional morphology in strigiform hind limbs.

Strigiformes are an order of raptorial birds consisting exclusively of owls: the Tytonidae (barn owls) and the Strigidae (true owls), united by a suite of adaptations aiding a keen predatory lifestyle, including robust hind limb elements modified for grip strength. To assess variation in hind limb morphology, we analysed how the dimensions of the major hind limb elements in subfossil and modern species scaled with body mass. Comparing hind limb element length, midshaft width, and robusticity index (RI: ratio of midshaft width to maximum length) to body mass revealed that femoral and tibiotarsal width scale with isometry, whilst length scales with negative allometry, and close to elastic similarity in the tibiotarsus. In contrast, tarsometatarsus width shows strong positive allometry with body mass, whilst length shows strong negative allometry. Furthermore, the tarsometatarsi RI scales allometrically to mass0.028, whilst a weak relationship exists in femora (mass0.004) and tibiotarsi (mass0.004). Our results suggest that tarsometatarsi play a more substantial functional role than tibiotarsi and femora. Given the scaling relationship between tarsometatarsal width and robusticity to body mass, it may be possible to infer the body mass of prehistoric owls by analysing tarsometatarsi, an element that is frequently preserved in the fossil record of owls.