The origin and expansion of biological diversity is regulated by both developmental trajectories1,2 and limits on available ecological niches3–7. As lineages diversify an early, often rapid, phase of species and trait proliferation gives way to evolutionary slowdowns as new species pack into ever more densely occupied regions of ecological niche space6,8. 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 unclear9. Here we address this problem on a global scale by analysing a novel crowd-sourced dataset of 3D-scanned bill morphology from >2000 species. We find that bill diversity expanded early in extant avian evolutionary history before transitioning to a phase dominated by morphospace packing. 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 Darwinian9 and Simpsonian4 ideas of microevolution within adaptive zones and accelerated evolution between distinct adaptive peaks.

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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.geometric morphometrics | integration | allometry | birds | modularity T he avian beak offers a classic example of adaptation to feeding ecology, with beak morphology frequently considered to represent evolutionary adaptation to specialized trophic niches [e.g., Galápagos finches (1), Hawaiian honeycreepers (2), and Madagascan vangas (3)]. Despite this axiom, we lack quantitative data on the degree to which skull and beak morphology is influenced not only by feeding ecology, but also by other sources of variation or constraint (4). Although the beak is often seen as the target of selection mechanisms closely allied to feeding ecology, such as prey type, feeding style, or beak use, evidence also suggests that beak morphology and variation may be constrained by a number of other factors, including evolutionary history (phylogeny) and development on the component parts of the entire skull. Breakthrough experiments in molecular genetics have shown that the mechanisms driving beak shape variation encompass modifications to the timing of expression of conserved developmental pathways (5-9), resulting in beak diversity described by a few relatively simple geometric transformations (10). However, pleiotropic associations between different skull structures can also contribute to the shape of the avian beak (11), and Sonic hedgehog signaling from the forebrain also relates to the spatial organization of, and changes to, face and beak shape (12)(13)(14). Furthermore, assessments of bird skull phenotypic variation suggest that beak morphology may evolve cohesively with cranial morphology (15,16). Size is also an important consideration when assessing morphological variation. Larger animals gene...