An integrative approach to understanding bird origins

Background The origin of birds is one of the most enduring and dramatic evolutionary debates. The hypothesis that the primarily small-sized birds are nested within a theropod dinosaur group that includes the gigantic Tyrannosaurus rex has been supported by strong fossil evidence, but until recently, several important issues remained unresolved, including the origins of feathers and flight, the “temporal paradox” (the coelurosaurian theropods occur too late in the fossil record to be ancestral to the Jurassic bird Archaeopteryx), and supposed homological incongruities (e.g., the suggested homologies of three fingers in tetanuran theropods are different from those of living birds). Recent discoveries of spectacular dinosaur fossils from China and elsewhere provide new information to address these issues, and also prompt numerous studies in disciplines other than paleontology that help explain how bird characteristics originated and evolved. Evolutionary history of selected bird features inferred from multidisciplinary data. Recent studies demonstrate that major bird characteristics have evolved in a sequential way, and many of them initiated transformation early in dinosaur evolution, with some approaching modern conditions well before the origin of birds, whereas others appear only near the origin of the crown group birds. Advances The discoveries of feathered dinosaur fossils from the Jurassic and Cretaceous sediments of China and elsewhere document a diverse range of feathers from monofilamentous feathers to highly complex flight feathers, which show a general evolutionary trend of increasing complexity leading to the cladogenesis of birds. The wide occurrence of foot feathers in Mesozoic theropods (i.e., short filamentous forms in relatively basal theropods and large vaned forms in derived theropods, including early birds) clarifies feather-scale relations and integumentary evolution pertinent to flight origins and also shows that bird flight likely had evolved through a four-winged stage. With numerous discoveries of well-preserved dinosaur fossils covering a wide range of geological periods, the morphological, functional, and temporal transition from ground-living to flight-capable theropod dinosaurs is now one of the best-documented major evolutionary transitions. Meanwhile, studies in disciplines other than paleontology provide new insights into how bird characteristics originated and evolved—such as feathers, flight, endothermic physiology, unique strategies for reproduction and growth, and an unusual pulmonary system. The iconic features of extant birds, for the most part, evolved in a gradual and stepwise fashion throughout theropod evolution. However, new data also highlight occasional bursts of morphological novelty at certain stages particularly close to the origin of birds and an unavoidable complex, mosaic evolutionary distribution of major bird characteristics on the theropod tree. Research into bird origins provides a model example of how an integration of paleontological and neontological data can be used to gain a comprehensive understanding of the complexity surrounding major evolutionary transitions and to set new research directions. Outlook A refined, more robust phylogeny will be imperative to move our studies forward. A larger data set will help to increase the accuracy of phylogenetic reconstructions, but better character formulation and more accurate scorings are imperative at the current stage. In terms of character evolution, an integrative approach combining paleontological, neontological, developmental, temporal, and even paleoenvironmental data is particularly desirable. Greater examination of fossils pertaining to molecular information is also a potentially fruitful avenue for future investigation. Evolutionary scenarios for various aspects of the origin of birds have sometimes been constructed from neontological data, but any historical reconstruction must ultimately be tested using the fossil record. Consequently, dense fossil sampling along the line to modern birds and better understanding of transitional forms play key roles in such reconstructions. Recent discoveries of spectacular dinosaur fossils overwhelmingly support the hypothesis that birds are descended from maniraptoran theropod dinosaurs, and furthermore, demonstrate that distinctive bird characteristics such as feathers, flight, endothermic physiology, unique strategies for reproduction and growth, and a novel pulmonary system originated among Mesozoic terrestrial dinosaurs. The transition from ground-living to flight-capable theropod dinosaurs now probably represents one of the best-documented major evolutionary transitions in life history. Recent studies in developmental biology and other disciplines provide additional insights into how bird characteristics originated and evolved. The iconic features of extant birds for the most part evolved in a gradual and stepwise fashion throughout archosaur evolution. However, new data also highlight occasional bursts of morphological novelty at certain stages particularly close to the origin of birds and an unavoidable complex, mosaic evolutionary distribution of major bird characteristics on the theropod tree. Research into bird origins provides a premier example of how paleontological and neontological data can interact to reveal the complexity of major innovations, to answer key evolutionary questions, and to lead to new research directions. A better understanding of bird origins requires multifaceted and integrative approaches, yet fossils necessarily provide the final test of any evolutionary model. Bird evolution: How birds took to the air Research on the origin and evolution of birds has gathered pace in recent years, aided by a continuous stream of new fossil finds as well as molecular phylogenies. Bird origins, in particular, are now better understood than those of mammals, for which the early fossil record is relatively poor compared with that of birds. Xu et al. review progress in tracing the origins of birds from theropod dinosaurs, focusing especially on recent fossil finds of feathered dinosaurs of northeastern China. They integrate current research on developmental biology and functional anatomy with the paleontological record, to show how key features of birds—feathers, wings, and flight—originated and evolved, and radiated from their dinosaur forebears. Science, this issue 10.1126/science.1253293