Quantifying integration and modularity of evolutionary changes in morphometric traits is crucial for understanding how organismal shapes evolve. For this purpose, comparative studies are necessary, which need to take into account the phylogenetic structure of interspecific data. This study applies several of the standard tools of geometric morphometrics, which mostly have been used in intraspecific studies, in the new context of analyzing integration and modularity based on comparative data. Morphometric methods such as principal component analysis, multivariate regression, partial least squares, and modularity tests can be applied to phylogenetically independent contrasts of shape data. We illustrate this approach in an analysis of cranial evolution in 160 species from all orders of birds. Mapping the shape information onto the phylogeny indicates that there is a significant phylogenetic signal in skull shape. Multivariate regression of independent contrasts of shape on independent contrasts of size reveals clear evolutionary allometry. Regardless of whether or not a correction for allometry is used, evolutionary integration between the face and braincase is strong, and tests reject the hypothesis that the face and braincase are separate evolutionary modules. These analyses can easily be applied to other taxa and can be combined with other morphometric tools to address a wide range of questions about evolutionary patterns and processes.

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...

The interplay of evolution and development has been at the heart of evolutionary theory for more than a century. Heterochrony—change in the timing or rate of developmental events—has been implicated in the evolution of major vertebrate lineages such as mammals, including humans. Birds are the most speciose land vertebrates, with more than 10,000 living species representing a bewildering array of ecologies. Their anatomy is radically different from that of other vertebrates. The unique bird skull houses two highly specialized systems: the sophisticated visual and neuromuscular coordination system allows flight coordination and exploitation of diverse visual landscapes, and the astonishing variations of the beak enable a wide range of avian lifestyles. Here we use a geometric morphometric approach integrating developmental, neontological and palaeontological data to show that the heterochronic process of paedomorphosis, by which descendants resemble the juveniles of their ancestors, is responsible for several major evolutionary transitions in the origin of birds. We analysed the variability of a series of landmarks on all known theropod dinosaur skull ontogenies as well as outgroups and birds. The first dimension of variability captured ontogeny, indicating a conserved ontogenetic trajectory. The second dimension accounted for phylogenetic change towards more bird-like dinosaurs. Basally branching eumaniraptorans and avialans clustered with embryos of other archosaurs, indicating paedomorphosis. Our results reveal at least four paedomorphic episodes in the history of birds combined with localized peramorphosis (development beyond the adult state of ancestors) in the beak. Paedomorphic enlargement of the eyes and associated brain regions parallels the enlargement of the nasal cavity and olfactory brain in mammals. This study can be a model for investigations of heterochrony in evolutionary transitions, illuminating the origin of adaptive features and inspiring studies of developmental mechanisms.