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.

Fig. 1. The phylogenetic distribution of ABO phenotypes and genotypes. Shown is a phylogenetic tree of primate species, with a summary of phenotypic/ genotypic information given in the first column, and the genetic basis for the A versus B phenotype provided in the second column (functionally important codons at positions 266 and 268 are in uppercase letters). See Dataset S1 for the source of information about phenotypes/genotypes. Only species with available divergence times are represented here (34 of 40). The phylogenetic tree is drawn to scale, with divergence times (on the x axis) in millions of years taken from ref. 29. OWM, Old World monkeys; NWM, New World monkeys. Under a model of convergent evolution, these data suggest that A is the ancestral allele, and a turnover (e.g., a neutral substitution) occurred on the branch leading to Old World monkeys. If instead, B were ancestral, all Old World monkeys would have had to serendipitously converge from ATG to TTG to encode a leucine, whereas all New World monkeys and hominoids would have had to converge to the CTG codon.

Secondary aquatic adaptations independently evolved more than thirty times from terrestrial vertebrate ancestors 1,2 . For decades, non-avian dinosaurs were believed to be an exception to this pattern. Only a few species have been hypothesized as partly or predominantly aquatic 3,4,5,6,7,8,9,10,11 . However, these hypotheses remain controversial 12,13 largely due to the difficulty of identifying unambiguous anatomical adaptations for aquatic habits in extinct animals. In this study, we demonstrate that the relationship between bone density and aquatic ecologies across extant amniotes provides a reliable inference of aquatic habits in extinct species.We use this approach to evaluate the distribution of aquatic adaptations among non-avian dinosaurs. We find strong support for aquatic habits in spinosaurids, associated with a remarkable increase in bone density, which precedes the evolution of more conspicuous anatomical modifications, a pattern also observed in other aquatic reptiles and mammals 14,15,16 .Spinosaurids are revealed to be aquatic specialists with surprising ecological disparity, including subaqueous foraging behavior in Spinosaurus and Baryonyx, and non-diving habits in Suchomimus.

The skull of living birds is greatly modified from the condition found in their dinosaurian antecedents. Bird skulls have an enlarged, toothless premaxillary beak and an intricate kinetic system that includes a mobile palate and jaw suspensorium. The expanded avian neurocranium protects an enlarged brain and is flanked by reduced jaw adductor muscles. However, the order of appearance of these features and the nature of their earliest manifestations remain unknown. The Late Cretaceous toothed bird Ichthyornis dispar sits in a pivotal phylogenetic position outside living groups: it is close to the extant avian radiation but retains numerous ancestral characters. Although its evolutionary importance continues to be affirmed, no substantial new cranial material of I. dispar has been described beyond incomplete remains recovered in the 1870s. Jurassic and Cretaceous Lagerstätten have yielded important avialan fossils, but their skulls are typically crushed and distorted . Here we report four three-dimensionally preserved specimens of I. dispar-including an unusually complete skull-as well as two previously overlooked elements from the Yale Peabody Museum holotype, YPM 1450. We used these specimens to generate a nearly complete three-dimensional reconstruction of the I. dispar skull using high-resolution computed tomography. Our study reveals that I. dispar had a transitional beak-small, lacking a palatal shelf and restricted to the tips of the jaws-coupled with a kinetic system similar to that of living birds. The feeding apparatus of extant birds therefore evolved earlier than previously thought and its components were functionally and developmentally coordinated. The brain was relatively modern, but the temporal region was unexpectedly dinosaurian: it retained a large adductor chamber bounded dorsally by substantial bony remnants of the ancestral reptilian upper temporal fenestra. This combination of features documents that important attributes of the avian brain and palate evolved before the reduction of jaw musculature and the full transformation of the beak.