Introduction

Among tetrapods, extant birds exhibit incredible taxonomic and ecomorphological diversity, comprising over 10,000 extant species that occupy myriad niches on 7 continents [1–3]. They possess a number of specialised traits that have been proposed as key innovations that facilitated their radiation, including the keeled pectoral girdle and flight stroke [4,5]; a hindlimb capable of perching [6]; a short, fused caudal axial skeleton [7]; an air-sac–based respiratory system [8]; an edentulous beak [9]; and highly encephalised brains [10,11] among other traits. Did this broad suite of phenotypic changes result in enhanced disparity and rates of phenotypic evolution in birds compared to their non-avian relatives? The rich fossil record shows that the stem group of birds, the non-avian dinosaurs, also exhibit remarkable variation in body plan, body size, and trophic ecology [12,13]. As such, understanding the context of avian diversification requires an in-depth investigation of the dynamics of tempo and mode of phenotypic evolution across Dinosauria as a whole [9,14–21].

Previous research comparing macroevolutionary patterns between avian and non-avian dinosaurs has focused on the post-cranial skeleton and/or body size [16–18,20,22–24]. Many of these studies have shown significant heterogeneity in disparity and evolutionary rates across dinosaur clades and across regions of the body. However, there remains some debate whether the radiation of crown birds represents a shift in tempo and mode of evolution or a continuation of existing trends. For example, some studies quantifying rates of phenotypic evolution across the origin of birds have recovered sustained high evolutionary rates across the entire avian stem lineage [18], while others have suggested that birds indeed evolve under different rates or adaptive regimes compared to non-avian dinosaurs [16,24]. Still others have found an isolated acceleration of evolutionary rate before the origin of birds, at the root of Paraves [17]. Despite this uncertainty about the timing of rate shifts in dinosaur macroevolution, there is an emerging consensus that there is heterogeneity in the tempo and mode of evolution across body regions [15,20] and across lineages [16–18,22].

Fewer studies have focused on the tempo and mode of craniofacial evolution specifically, despite many of the key ‘avian’ features being localised to the skull (e.g., edentulous beak, kinetic palate, encephalised brain). These studies have primarily been limited to the use of linear or two-dimensional (2D) morphometric data. These analyses support the idea that avian cranial diversity is aligned along a similar axis of variation as in non-avian dinosaurs, with similar trends in braincase to face proportions [25]. However, these efforts have largely been restricted to Theropoda [21,26–28], excluding much of total non-avian dinosaur diversity.

Analysis of avian cranial skeletal evolution using three-dimensional (3D) morphometric data has revealed a mosaic pattern of evolution [29]. The components of the skull evolve at different tempo and mode, with high rate variability among lineages [29,30]. Rate and disparity are positively correlated, with the anterior face evolving fastest and achieving the highest disparity. In contrast, the posterior and ventral braincase evolves relatively slowly and has low variance. This heterogeneity in rate and disparity across skull regions supports the hypothesis that the mosaic assembly of the avian skull has contributed to the vast phenotypic and ecological disparity within the clade [29,31]. Birds and non-avian dinosaurs exhibit some similarities in cranial integration patterns, further suggesting that avian cranial variation forms a continuum with other members of Dinosauria. For example, the regions that are strongly integrated in birds, such as the occiput, are also highly integrated in non-avian dinosaurs [32]. However, it is currently unknown whether these common integration patterns across Dinosauria reflect similar patterns of mosaicism in avian and non-avian dinosaurs.

Here, we test whether the origin of birds is marked with a distinct shift in cranial evolutionary dynamics. Specifically, we assess how the macroevolutionary patterns generating avian cranial diversity compares to those giving rise to the diversity of cranial morphology across Dinosauria as a whole. We address 2 main questions. First, did the same regions of the skull evolve at high rates and exhibit high disparity in non-avian dinosaurs as in birds? We hypothesise that because of the major differences in cranial anatomy, function, development, and phenotypic integration, non-avian and avian dinosaurs exhibit distinct patterns of regionalisation of variability within the skull. Second, do birds and non-avian dinosaurs evolve at different rates? Previous studies quantifying cranial form across dinosaurs and birds have relied on limited length measurements or a small set of 2D landmarks because of limited points of clear homology [21,26–28]. To comprehensively represent the complex morphology and diversity of the dinosaur skull, we used a high-dimensional 3D geometric morphometric approach to quantify shape morphology across the entire surface of the skull in both extant birds (n = 354) and non-avialan dinosaurs (n = 36), as well as the Cretaceous ornithuran bird Hesperornis. Using semiautomated placement of surface semi-landmarks [33], we projected a total of 775 surface semi-landmarks onto each specimen (S1 Fig), allowing for the disparate morphology of non-avian and avian dinosaurs to be compared in a single unified Procrustes space [33]. Because this study concerns 3D shape of the entire skull, we selected only highly complete, articulated, and undeformed fossil specimens. We also included several specimens that were digitally reconstructed, restored, or retrodeformed [34–37]. Although these requirements reduced the total number of extinct taxa in the dataset, it also maximised the quality of the data and minimised missing data. This dataset contains representatives of all major groups, including 4 sauropodomorphs, 4 thyreophorans, 4 hadrosaurs, 3 pachycephalosaurs, 5 ceratopsians, and 15 non-avian theropods S2 Table). Although the total sampling in this study represents only a fraction of the overall diversity of dinosaurs, the sampling is proportionate for avian and non-avian dinosaurs, representing approximately 3% of known species. We sample over 80% of extant avian families, with non-avian sampling covering most major clades and the breadth of cranial variation. Moreover, the total number of specimens in the present analysis is similar to or exceeds the taxonomic sampling of other analyses of cranial shape in dinosaurs or birds, all of which use a much less detailed characterisation of morphology with 2D geometric morphometrics (e.g., n = 22 [21], n = 36 [27], n = 41 [28], n = 108 [26]). We additionally carried out post hoc analyses, detailed below, to test for statistical artefacts related to sampling.

Because of the variable completeness of the fossil specimens, we conducted all analyses concerning rate and disparity of a region (e.g., a whole bone or phenotypic module composed of multiple bones) using all specimens that preserve that region or element. For analyses concerning rate and disparity across the entire skull, we performed tests using 2 subsets of the total sample: one consisting of those taxa that preserve the dorsal and lateral sides of the skull (n = 28) and composed of 9 anatomical modules (S2 Table) and the other consisting of those taxa preserving the occiput and quadrate as well (11 anatomical modules, n = 19). We then used modern comparative methods to estimate phenotypic rates of evolution across time, taxa, and cranial regions.

Results

Under a variable-rates Brownian Motion (BM) model [38], all cranial regions evolved more slowly in birds than in either non-avian theropods, non-theropod dinosaurs (sauropodomorphs and ornithischians), or both (Fig 1 and S2–S22 Figs). The distribution of rates is highly variable across cranial regions and across taxa, but the highest rates are consistently observed on branches within non-avian dinosaurs rather than those within birds. These results are robust to the choice of phylogenetic topology and tree dating approach. Comparing per-branch evolutionary rate scalars demonstrates that birds evolved significantly more slowly than non-avian theropods and non-theropod dinosaurs in all cranial regions (Fig 2). These results are robust to taxonomic subsampling (S37 Fig) and changes in Procrustes alignment (S38 Fig) and are further supported by rate comparisons using the multivariate K (σ_mult) rate statistic [39] that assumes equal-rates BM (S39–S42 Figs, S1 Table)

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Fig 1. Estimation of rates of cranial evolution on a time-calibrated phylogeny of Dinosauria using a variable-rates BM model of evolution.

(A) In the rostrum, ornithischians evolved faster than avian and non-avian theropods. (B) The cranial vault evolves fastest in non-avian dinosaurs with bony cranial ornaments. (C) Rates of evolution are generally conserved and low in the occipital region, with slightly elevated rates in Passeriformes and in pachycephalosaurs. Black triangle indicates the origin of Aves. See S2–S36 Figs for estimated rates for all cranial regions and phylogenetic hypotheses and detailed tip labels. Data and code archived at www.github.com/rnfelice/Dinosaur_Skulls. BM, Brownian Motion.

https://doi.org/10.1371/journal.pbio.3000801.g001

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Fig 2. Comparison of per-group evolutionary rate scalars.

Birds do not have the highest rates of evolution in any cranial region. For each group, mean rate scalar is the mean of the rate scalars in the post-burn-in posterior distribution under the variable-rates evolutionary model estimated using BayesTraits under the traditional Dinosaur phylogenetic hypothesis (Saurischia and Ornithischia as sister clades). Mean rates were scaled to the sum of the branch lengths in the corresponding subtree. Mean rate scalars were compared between groups using non-parametric t tests; significantly different distributions are indicated with ****p < 0.00005. These results are robust to subsampling of taxa (S1 Fig 37), Procrustes superimposition (S1 Fig 38) and alternative methods for comparing evolutionary rates (S39–S42 Figs). Data and code archived at www.github.com/rnfelice/Dinosaur_Skulls.

https://doi.org/10.1371/journal.pbio.3000801.g002

For each skull region, variable-rates evolutionary models illustrate which subclades are driving the differences in rates between non-avian dinosaurs and birds (Fig 1). In the rostrum (premaxilla, maxilla, nasal, jugal), rapid evolution is particularly evident in Diplodocus and Lambeosaurus, which convergently have distinct cranial configurations with posterodorsally positioned nasals and elongate premaxillae compared to their closest relatives in this analysis (Fig 1A and S2–S4 Figs). Among non-avian theropods, the oviraptorosaurs Citipati and Incisivosaurus have relatively high rates of rostrum evolution. Although they represent sister taxa in our sampling, these 2 genera exhibit widely divergent cranial morphotypes (e.g., Citipati has an edentulous premaxilla, unlike Incisivosaurus). Along the early avialan lineages (including Hesperornis), rates of rostrum evolution are slightly higher, but the rates along the branch leading to crown Aves and basal branches within the crown group are relatively slow compared to non-avian dinosaurs.

Within non-avian dinosaurs, evolutionary pulses in the cranial vault are associated with cranial ornaments. Ornithischian dinosaurs, such as horned and crested ceratopsians and dome-headed pachycephalosaurs, exhibit elevated rates for this region (Fig 1B and S5–S7 Figs). Similarly, high rates are seen within non-avian Theropoda, where parietal crests are present in taxa such as Tyrannosaurus and Allosaurus, although these structures are related to muscle attachment rather than display [40]. These bony elaborations of the skull roof are relatively rare in birds [41]. However, per-bone analyses limited to non-avian dinosaurs indicate that rate heterogeneity in the vault is driven not only by ornamentation. Indeed, several unornamented theropods also exhibit high rates of vault evolution on terminal branches, including those leading to Ornithomimus, Struthiomimus, and Incisivosaurus (S5–S7 Figs). In the frontal, non-avian theropods underwent faster evolution compared to ornithischians (S23 Fig), although the ceratopsids Triceratops, Chasmosaurus, and Diabloceratops also exhibit high evolutionary rates in the frontal, presumably reflecting the reorganisation of the skull roof to support the postorbital horns present in these species. In contrast, the parietal evolved faster in ornithischians than in saurischians (S24 Fig). The slowest-evolving ornithischians are relatively unornamented (e.g., Stegosaurus, Thescelosaurus, and Pinacosaurus), and theropods with fast-evolving parietals are tyrannosaurids with parietal (nuchal) crests (e.g., Tyrannosaurus, Teratophoneus, and Alioramus). As with the parietal, the squamosal generally evolved fastest in ornithischians and slowly in saurischians (S25 Fig).

The quadrate and pterygoid form a strongly integrated unit with relatively slow evolutionary rates in crown birds [29]. In contrast, the quadrate exhibits high rates across non-avian dinosaurs in the 11-module analyses (Fig 3C). However, when analysed separately from other skull elements, such that only shape—rather than both shape and relative position—is represented, the quadrate exhibits apparently low evolutionary rates in non-avian dinosaurs than in crown birds (S14–S16 Figs). Indeed, quadrate shape evolution is slow among non-avian dinosaurs, except in ornithomimosaurs and Plateosaurus (S14–S16 Figs). This difference reflects the effects of Procrustes alignment with other components of the skull, which preserves information about relative positions of elements, compared to separate Procrustes alignments for each element that characterises only the shape of the region of interest. When σ_mult rate comparison tests are carried out on the quadrate landmarks from the global Procrustes alignment, non-avian dinosaurs exhibit significantly faster evolution than birds (S42 Fig). The aspect of the quadrate that evolves rapidly in non-avian dinosaurs, therefore, seems to be the relative position of the articular surface of the quadrate relative to the rest of the skull, rather than its shape. In contrast, the pterygoid shows a high rate of evolution along the branch leading to Avialae (S17–S19 Figs). This suggests that the derived, strut-like pterygoid of birds and concomitant loss of the ectopterygoid evolved rapidly immediately preceding the origin of the crown group. Among non-avian dinosaurs, there is an increase in evolutionary rate of the pterygoid at the origin of each of the major clades (Theropoda, Sauropodomorpha, and Ornithischia) and Ornithomimosauria.

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Fig 3. Per-landmark evolutionary rates (under single-rate BM model) and Procrustes variance.

Landmarks and sliding semi-landmarks represented in the 9-module dataset (A, B) and 11-module dataset (C, D), illustrated on the skull of Erlikosaurus andrewsi (IGM 100/111). Landmarks are coloured according to evolutionary rate (A, C) and Procrustes variance (B, D), where a warmer colour indicates greater value. Data and code archived at www.github.com/rnfelice/Dinosaur_Skulls. BM, Brownian Motion; IGM, Paleontological Center, Mongolian Academy of Sciences.

https://doi.org/10.1371/journal.pbio.3000801.g003

The occiput shows slow rates of evolution in both birds [29] and non-avian dinosaurs (S8–S10 Figs), a feature that may be conserved across tetrapods [42,43]. Nonetheless, ornithomimosaurs show bursts of rapid evolution in the occiput, driving its evolution to be higher in non-avian theropods than crown birds (Figs 1C and 2, S8–S10 Figs). High rates of occipital evolution are also present in pachycephalosaurs, reflecting their derived occipital morphology which has been interpreted as supporting increased epaxial cervical musculature, hypothesised as an adaptation for their inferred headbutting behaviour [44,45].

Examining patterns of disparity and evolutionary rates across the skull demonstrates major differences in how the skull evolved in in non-avian and avian dinosaurs. Non-avian dinosaurs show high rates of evolution predominantly in the posterodorsal parts of the skull. This pattern contrasts with birds, which have the highest rates of evolution in the anterior-most parts of the face [46]. In the 9-module dataset, per-landmark evolutionary rates show that the fastest evolving region—the parietal (S43 Fig, σ_mult = 4.53 × 10⁻⁷)—evolves approximately 2.7 times faster than the slowest-evolving modules: the frontal and the lacrimal (frontal: σ_mult = 1.64 × 10⁻⁷; lacrimal: σ_mult = 1.69 × 10⁻⁷). This difference reflects the inclusion of a larger sample of ceratopsians in that dataset, which possess elaborate frills formed by the parietal and squamosal (Fig 3A). The squamosal and the quadratojugal show moderately high rates, and the remainder of the skull evolves relatively slowly (Fig 3A).

Skull shape disparity, as calculated by Procrustes variance, exhibits similar patterns to rates across the skull, where regions that evolved rapidly are also the most disparate. The fast-evolving parietal and quadratojugal exhibit the highest variance, whereas the frontal and lacrimal + prefrontal have the lowest variance across avian and non-avian dinosaurs (Fig 3). In all regions except the quadrate, birds have significantly lower disparity than non-avian dinosaur groups (S44 Fig, S2 Table and S3 Table), which is congruent with the pattern observed with evolutionary rates.

In the 11-module dataset with fewer specimens represented (notably, excluding ceratopsians) the parietal and quadratojugal retain high evolutionary rates (Fig 3C and S43 Fig), as observed in the 9-module dataset. The other parts of the skull exhibit greater variation in rates compared to the 9-module dataset. The quadrate underwent the highest rate of evolution, and the frontal, nasal, premaxilla, palatal surface of the maxilla, and prefrontal also evolved rapidly. In contrast, the occiput, postorbital, squamosal, ventral lacrimal, and dorsal maxilla evolved slowly (Fig 3C and S43 Fig).

To further illustrate the evolutionary mosaicism across the cranial regions and taxa, we calculated the distance from the mean skull shape for each specimen in the 11-module dataset for each landmark (Fig 4). In non-avian theropods, the region of highest phenotypic change is typically the rostrum (Fig 4). In some theropods (Citipati, Tyrannosaurus, Allosaurus, and Majungasaurus), the quadrate and quadratojugal are also very different from the average non-avian dinosaur skull shape. In ornithischians, the largest amount of phenotypic change is typically localised to the circumorbital bones and the cranial vault (Fig 4). Notably, ankylosaurs (Pawpawsaurus and Panoplosaurus) and Stegosaurus, like non-avian theropods, exhibit a large amount of phenotypic change in the premaxilla. Unlike theropods, however, the maxilla has low Procrustes distance from the mean in these taxa. Due to its prominent frill, the region with the highest magnitude of change in Protoceratops is the posterior parietal. Unexpectedly, the prosauropod Plateosaurus most closely resembles the pattern of cranial variation typical of Theropoda, with the greatest deviations from the average dinosaur skull observed in the face and jaw joint. Sauropods, in contrast, exhibit a different pattern. Camarasaurus is characterised by a large amount of phenotypic change in the vault, lacrimal, and ventrolateral margin of the skull. In contrast, Diplodocus, with its distinctive anteroposteriorly elongate face, has the ventral margin of the premaxilla, maxilla, and jugal as regions of greatest change.

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Fig 4. Phenotypic difference between each specimen for each landmark in the 11-module dataset and the mean skull shape.

For each specimen, the mean landmark configuration is plotted with points coloured relative to the Procrustes distance between the position of that point in the mean shape and in that specimen. Warmer colours denote landmarks having higher displacement from the mean, and cooler colours are more similar to the mean shape. Data and code archived at www.github.com/rnfelice/Dinosaur_Skulls.

https://doi.org/10.1371/journal.pbio.3000801.g004

Discussion

The patterns of cranial shape evolution exhibited by birds do not reflect those of the other dinosaur groups. Despite their ecomorphological diversification, birds display slower rates of evolution than non-avian dinosaurs in almost all cranial regions. The regions of the dinosaur skull that have experienced the highest rates of evolution and achieved the highest disparity differ across clades and largely reflect clade-specific anatomical specialisations, including elaborate skull ornamentations. Whereas the fastest evolving part of the avian skull is the anterior rostrum [29,46], this is not the case for all dinosaurs. Collectively, non-avian dinosaurs have high rates of evolution in the cranial vault and the relative position of the jaw joint.

We propose that these regions have experienced rapid evolutionary change in non-avian dinosaurs, but not birds, for several reasons. First, rapid evolution in the parietal and squamosal are attributed to the diverse cranial ornaments that occur across theropods and marginocephalians. Bony ornamental structures are uncommon in extant birds, with most cranial display in birds being achieved through soft tissue and feathers [41]. However, the few birds with bony crests have previously been shown to exhibit rapid evolution in the skull roof [29]. Ornamental structures, whether they evolve through sexual selection, for species recognition, or for some other function [47,48], are presumably under more intensive phenotypic selection and are expected to show high rates of evolution and high variability. However, the presence of display structures alone cannot explain high rates of vault evolution in non-avian dinosaurs, as many unornamented taxa exhibit rapid phenotypic evolution in this region.

Another possible driver of phenotypic variation and rapid evolutionary change in the vault in non-avian dinosaurs is the structure and function of the adductor chamber. The squamosal and parietal contribute to the borders of the superior temporal fenestra, through which several major jaw muscles pass. These include the m. adductor mandibulae externus profundus, medialis, and superficialis, jaw closing muscles that originate on the temporal fossa and temporal bar [49]. The shape of these vault elements thus determines both the size of the jaw adductor apparatus and therefore foraging performance and behaviour. Like the vault, the quadratojugal shows high evolutionary rates and disparity (Fig 3). This element is also linked to food acquisition and processing; as in the squamosal, the dorsoventral length of the quadratojugal relates to the total height of the adductor chamber and thus the length and functional properties of the associated jaw adductor muscles. Furthermore, in some clades (tyrannosaurs, hadrosaurs), the pterygoideus ventralis muscle attaches to the jugal, further emphasising the importance of shape variation in this region for jaw function [49].

In non-avian dinosaurs, the quadrate exhibits the highest evolutionary rate in the 11-module dataset (Fig 3) in contrast to birds, which show very low evolutionary rates for the quadrate [29]. The position, orientation, and shape of the articular surface of the quadrate has important implications for mechanical advantage and range of motion of the jaw joint proper and thus jaw function. Similarly, snakes exhibit high disparity and rates in the quadrate, reflecting functional variation in their highly kinetic skulls, especially in comparison to other members of Squamata [42]. The rapid evolution of disparity in the quadrate in non-avian dinosaurs may similarly reflect variation in jaw function. A variety of complex “chewing” mechanics independently evolved across ornithischian clades, including ceratopsians, ankylosaurs, and hadrosaurs, with a wide range of occlusal patterns and power strokes [50–54]. Likewise, feeding mechanics are variable in Theropoda, with hyper-carnivorous, bone-crushing, edentulous, and herbivorous forms [13,37,55,56]. There is much less biomechanical variation in jaw joint function in extant birds, although there is variation in cranial kinesis mechanics within Neoaves [57,58]. As such, the higher rates and disparity of both the adductor chamber region and the jaw joint in non-avian dinosaurs are likely associated with their high variation in jaw biomechanics and food processing strategies.

Variation in food acquisition and processing mechanisms may also have driven differences in rate and disparity in the anterior face across Dinosauria. In birds, the anterior rostrum is the most rapidly evolving and variable part of the skull [29]. However, the mean rate scalar in non-theropod dinosaurs is more than 2 times higher than in avian and non-avian theropods. This theropod/non-theropod split is partly due to high variation in the nasal bone, which is ornamented in some ceratopsians and Lambeosaurus or contributes to unusually positioned nares as in sauropods such as Diplodocus. However, rapid rostrum evolution in non-theropod dinosaurs is primarily driven by the premaxilla, which evolves slowly in most non-avian theropods but much faster in most ornithischians. The non-avian theropods that do achieve high rates of premaxilla evolution are those with edentulous premaxillae and/or rhamphotheca, including ornithomimosaurs and Citipati (S26 Fig and S27 Fig). Similarly, taxa with edentulous premaxillae (hadrosaurs, ceratopsians) have high rates of evolution within Ornithischia.

In birds, the evolution of an edentulous beak is part of a suite of cranial traits, including increased encephalisation and orbit size, that have been linked with the transition to a more paedomorphic cranial phenotype [9,10,21,59–61]. The evolution of this derived neurocranial morphology, emphasising brain size and visual acuity, could have then constrained the potential for variation related to other neurocranial functions, including jaw musculature and bony ornaments. Conversely, non-avian dinosaurs with low encephalisation [62] would not experience this constraint and therefore would be able to rapidly evolve diverse neurocranial and jaw joint phenotypes (although note that some non-avian dinosaurs, like birds, were relatively highly emphasised, see [11]).

These observed differences in rates and disparity among dinosaur groups may be influenced in part by the particular sampling strategy employed in this study. Some clades are under-sampled due to lack of adequately preserved specimens, including Sauropoda and basal members of Avialae. Including additional taxa in future analyses will surely improve our understanding of the tempo and mode of trait evolution. However, our diagnostic analyses of branch length heterogeneity and the relationship between branch length and evolutionary rate suggests that the higher rates observed in non-avian dinosaurs are not an artefact due to gaps in sampling but are in fact biological patterns.

Each cranial region evolves relatively slowly in birds, suggesting that birds, despite some being considered an icon of adaptive radiations, did not achieve their extant cranial diversity through extraordinarily high rates of evolutionary change. The higher rates and disparity of cranial shape evolution in non-avian theropods, especially in the posterior skull (vault, occiput, and pterygoid), starkly contrasts with previous studies comparing disparity and evolutionary rates in the postcranial skeleton of birds and non-avian dinosaurs. Birds have significantly greater disparity in limb proportions [15,19] and higher rates of limb evolution [15,18,22] than non-avian theropods. Similarly, analysis of rates of evolution using discrete morphological characters have demonstrated that the skeleton, as a whole, evolves faster in Avialae than in other theropods [16]. Different conclusions about the relative evolutionary rates of birds in the present analysis and previous studies exemplify the mosaic evolution of birds [29]. The modular organisation of the avian skeleton allows different regions of the body to evolve at different rates in response to different selective pressures, and different tempo of evolution between regions of the theropod skeleton have been demonstrated previously [19,20,63]. While some previous analyses of phenotypic evolution in theropods have included cranial traits and concluded that birds evolve significantly faster than other theropods, these works did not partition traits according to region (e.g., cranial versus forelimb versus hindlimb) [16,18]. As such, high rates of evolution in the limbs may overwhelm low rates of evolution in the skull, generating an overall pattern of rapid phenotypic change in birds.

As birds were experiencing high rates of evolution in the postcranial skeleton and using their newfound variation in limb morphology to exploit a variety of habitats, their cranial evolution had slowed down relative to other dinosaurs. Whether this is related to the biomechanical demands of aerial locomotion or encephalisation, developmental factors caused by reorganisation of the palate and vault, or phylogenetic inertia, birds failed to achieve the high rates of cranial evolution observed in non-avian dinosaurs. While the wings [22,63], hindlimb [64], and axial skeleton [65–67] rapidly achieved high disparity, cranial diversity decelerated compared to the diversity that was once present across Dinosauria, reinforcing that avian morphology and disparity are the product of mosaic evolution.

Methods

Supporting information

Acknowledgments

Thanks are due to those who contributed scan hot: A. Knapp, J. M. Bourke, C. Early, and T. Green. D. F. Wright and D. J. Button provided guidance on tip-dating methods. We also thank the curators and collections managers who facilitated specimen scanning: J. White, C. Lefevre, A. Herrel, C. Milensky, M. Brett-Surman, C. Mehling, D. Kizirian, J. Maisano, P. Holroyd, S. Rogers, W. Simpson, B. Marks, J. Hinshaw, P. Sweet, L. Garetano, J. Rosado, K. Zyskowski, G. Watkins-Colwell, J. Scanella, A. Henrici, B. Sanchez, B. Strilisky, C. Sidor, M. Rivin, and C. Levitt.