Current Biology


The Origin and Diversification of Birds
Stephen L. Brusatte1,*, Jingmai K. O’Connor2,*, and Erich D. Jarvis3,4,*
1School of GeoSciences, University of Edinburgh, Grant Institute, King’s Buildings, James Hutton Road, Edinburgh EH9 3FE, UK
2Instituteof Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China
3Department of Neurobiology, Duke University Medical Center, Durham, NC 27710, USA
4Howard Hughes Medical Institute, Chevy Chase, MD 20815, USA

*Correspondence: (S.L.B.), (J.K.O.), (E.D.J.)

Birds are one of the most recognizable and diverse groups of modern vertebrates. Over the past two de-
cades, a wealth of new fossil discoveries and phylogenetic and macroevolutionary studies has transformed
our understanding of how birds originated and became so successful. Birds evolved from theropod dino-
saurs during the Jurassic (around 165–150 million years ago) and their classic small, lightweight, feathered,
and winged body plan was pieced together gradually over tens of millions of years of evolution rather than in
one burst of innovation. Early birds diversified throughout the Jurassic and Cretaceous, becoming capable
fliers with supercharged growth rates, but were decimated at the end-Cretaceous extinction alongside their
close dinosaurian relatives. After the mass extinction, modern birds (members of the avian crown group)
explosively diversified, culminating in more than 10,000 species distributed worldwide today.

Introduction dinosaurs Dromaeosaurus albertensis or Troodon formosus. This
Birds are one of the most conspicuous groups of animals in the clade includes all living birds and extinct taxa, such as Archaeop-
modern world. They are hugely diverse, with more than 10,000 teryx and Enantiornithes. Some researchers refer to this group as
extant species distributed across the globe, filling a range of Avialae (e.g. [2,5]), but others use the name Aves (e.g. [6]). In this
ecological niches and ranging in size from the tiny bee humming- review, we avoid these debates by referring to this group as ‘Avi-
bird (2 grams) to the ostrich (140,000 grams). Their feathered alae/Aves’ and its members as ‘avians’. We use Neornithes to refer
bodies are optimized for flight, their supercharged growth rates to the avian crown group, which comprises all living birds and the
and metabolism stand out among living animals, and their large descendants from their most recent common ancestor.
brains, keen senses, and the abilities of many species to imitate
vocalizations and use tools make them some of the most intelli- The Dinosaur–Bird Link: Once Controversial, Now
gent organisms on the planet [1]. Mainstream
This begs a fascinating question: how did birds achieve such What did birds evolve from and where do they fit into the family
great diversity and evolutionary success? For much of the last tree of life? For much of the 19th and 20th centuries these ques-
two centuries this was a mystery, but over the past two decades tions were hotly debated. The first hint that birds evolved from
a wealth of new fossil discoveries, molecular phylogenetic ana- reptiles appeared in 1861, only a few years after Darwin pub-
lyses of living birds, and quantitative macroevolutionary analyses lished On the Origin of Species, with the discovery of an exquisite
have revolutionized our understanding of bird origins and evolu- skeleton of a Late Jurassic (ca. 150 million year old) bird from
tion. This new information reveals a surprising story: birds Germany. Named Archaeopteryx by British anatomist Richard
evolved from dinosaurs and have a deep evolutionary history, Owen, this fossil possessed a curious mixture of classic bird fea-
during which their signature body plan evolved piecemeal over tures, such as feathers and wings, but also retained sharp claws 
100 million years of steady evolution alongside their dinosau- on the hands, a long bony tail, and other reptilian characteristics
rian forebears before many of the modern groups of birds explo- [7]. Over the next two decades, Thomas Henry Huxley — Owen’s
sively diversified after the non-avian dinosaurs went extinct 66 great rival and Darwin’s most vociferous early supporter —
million years ago (Figure 1) (e.g. [2–4]). argued that Archaeopteryx bore remarkable similarities to small
The origin of birds is now one of the best understood major dinosaurs like Compsognathus, supporting an evolutionary link
transitions in the history of life. It has emerged as a model case between the groups [8,9]. This idea gained some acceptance,
for using a combination of data from fossils, living species, gene- but fell out of favor during the early 20th century, largely as a
alogies, and numerical analyses to study how entirely new body result of an influential book by Danish anatomist Gerhard
plans and behaviors originate, and how prominent living groups Heilmann [10]. Up until the 1960s most scientists held that birds
achieved their diversity over hundreds of millions of years of evo- originated from a nebulous ancestral stock of reptiles called
lution [2,3]. Here, we review what is currently known about the ‘thecodonts’.
origin, early diversification, and rise to dominance of birds, and The debate over bird origins was reinvigorated in the 1960s–
the various lines of evidence that piece together this story. 1980s, as a new generation of paleontologists spearheaded
Note that throughout this review, we use the vernacular term the ‘Dinosaur Renaissance’ [11]. John Ostrom discovered fossils
‘birds’ to refer to a specific group, which is defined in a phyloge- of the astonishingly bird-like dinosaur Deinonychus in western
netic sense as the most inclusive clade containing Passer North America [12], Robert Bakker and colleagues argued that
domesticus (the house sparrow) but not the extinct bird-like dinosaurs grew fast and had active metabolisms like living birds

R888 Current Biology 25, R888–R898, October 5, 2015 ª2015 Elsevier Ltd All rights reserved

However. Dinosauria Simple filamentous feathers Michael Keesey. Cz.24–26]. and secondly. convincing most of the remaining related to birds than the other [2. ically to primitive dromaeosaurids and troodontids. Manir. the same way that humans are a type of mammal (Figure 1). and how the transition between non-bird dinosaurs and birds maeosaurids. Andrew A.22]. with the two The iconic Archaeopteryx is still widely considered to be among groups linked by hundreds of shared features of the skeleton. The phylogeny shows where birds fit into the larger es es rm vertebrate family tree and the relationships of the rm ae ifo ri a ifo ri d ith earliest birds and their closest dinosaurian rela- s es x au op ns ru ry ae ith rn oo sau ith am ns os a au te ds es s s Sa iuso rn id hi s is En nis tives (based on [2] and other studies cited therein). ‘Bipedal posture’ silhouette by Amniota Tetrapoda Scott Hartman. Species silhouettes at the top of the image are 163 Jurassic sternum from phylopic. Scott Hart- Triassic man. Anne Claire Fabre.3. even by orni. reproduction. Birds These debates will likely continue. The fact the mostly small-bodied. and therefore are dinosaurs. Matt 237 Saurischia Martyniuk. Where Birds Nest in the Dinosaur Family Tree long-fingered scansoriopterygids are basal-most birds or non- Birds evolved from dinosaurs. but many ornitholo. and close dromaeosaurid and troodontid and Troodon [21.28]. to be the earliest than lizards or crocodiles (Figure 3). or whether one of them is more closely dinosaur–bird link [15–17]. 250 Archosauria Diapsida Michael Keesey. Steven Traver. Farke. so it is diffi- gists remained skeptical. The discovery in the late 1990s in China cult to tell them apart.29]. birds [24.J. J. that the oldest birds and their closest ever-more exclusive theropod subgroups: Coelurosauria. winged.24]. Matt Martyniuk. le ni n ia op or al os o o nt c ith ro rn r di or ib s ae tio is m pt or ae na do nn rd c pe lo co rn ph hy ith ra fu an m ur pe Timescale values are in millions of years.19–22]. Michael Keesey. long- aptora. This means that there is skeptics (Figure 2A–C). Current Biology 25. T. and Jacques Gauthier and colleagues used the revolution. just how bird-like some non-bird dinosaurs were (Figure 3). the first birds [2. Michael Keesey. lightweight. Their very closest relatives are armed. Michael Keesey.5. Scott Hartman.5. cir- cles represent species known from a particular Cretaceous point in time. earliest birds from their closest dinosaur relatives illustrates raptor [23]. such as Anchiornis and Xiaotingia. 201 Theropoda/Coelurosauria Vaned feathers Brad McFeeters/T. Stephen O’Connor/T.24–26.Current Biology Review Figure 1. October 5.5. that birds evolved from dinosaurs [18]. and feathered animals (Figure 4A. Thus. much more bird-like species such as Velociraptor. it is now known that many non-bird dinosaurs [27. There is also debate about whether the bizarre. dro. and behavior [2. Anchiornis. Nobu Tamura/T. Silhouette anatomical fea- Pygostylia tures in the lower part of the figure are plotted 145 approximately where they evolve on the phylog- Avialae/Aves (Birds) Keeled eny. 2015 ª2015 Elsevier Ltd All rights reserved R889 . It is now widely accepted. thologists. Deinonychus. T. the exact relationships among paravians (birds. Tyrannosaurus and Allosaurus. Xiaotingia. that birds of mostly carnivorous species that includes the behemoths first appear in the fossil record during the Middle–Late Jurassic. Mathew Wedel. sparrow-to-pigeon-sized. but also smaller and obviously around 165–150 million years ago (the age of Archaeopteryx. growth. Summary phylogeny (genealogical tree) of birds. the major subgroup swers do not change two important points: firstly. thick line sections of branches indi- 100 Ornithurae cate direct fossil evidence and thin lines are tem- poral distributions implied by phylogenetic ghost 120 Ornithuromorpha lineages. Matt Martyniuk. By the 1990s the vast majority of paleon. Matt Martyniuk. because as more fossils are found it is tree of dinosaurs [14]. there is current debate about of fossils from thousands of bona fide dinosaurs covered in whether dromaeosaurids and troodontids form their own clade feathers provided the most definitive visual evidence for the of close bird relatives. Additional studies have also found other small feathered were feathered and would have looked much more like birds theropods. large-brained dromaeosaur. becoming clear that the earliest birds were very similar anatom- tologists accepted the dinosaur–bird and designed by (from left to Paraves Pygostyle 174 Wings (fused tail) right): Nobu Tamura. relatives were small (roughly chicken-sized). that scientists are having a difficult time distinguishing the ids and troodontids. exemplified by the well-known Veloci. and troodontids) are uncertain and often vary was gradual. thick red za ho ch ro ra eo es ro ht Am on rn vi ro Sa Vo M Li Ty Je Ar C Tr O Ic N H O D C line denotes the mass extinction at the Creta- Cz ceous–Paleogene boundary caused by asteroid impact (denoted by fireball on the right). in bird maniraptorans [2. Michael Maniraptora Keesey. Birds are members of a nested set of relatives). arrows 66 denote lineages that survived the extinction. R888–R898. Harrison/T. Matt Martyniuk. but the alternative an- are nested within the theropod dinosaurs. Scott Furcula (wishbone) Hartman. between competing phylogenetic analyses based on morpho- ary new technique of cladistics to place birds within the family logical characters. feathered. Cenozoic interval after the end- 130 Ornithothoraces Cretaceous extinction.26]. also ongoing debate about which fossils are the earliest birds. but some studies have suggested that soft tissues.B). and Paraves (Figure 1). more primitive than Archaeopteryx. Bipedal posture Hinge-like ankle Current Biology [13]. it may instead be a primitive dromaeosaurid or troodontid Most amazingly.

such as a keeled sternum (breastbone). close relatives are Ichthyornis. and to the Late Cretaceous. include such taxa as Gobipteryx Birds had diversified by the Early Cretaceous. (B) The small long- armed dromaeosaurid cf. ceous [36]. semiaquatic taxa. elongate cora- coid. the beaked Confu- ciusornithiformes (a clade of early birds including the abundantly found Confu- ciusornis). and the Hesperornithiformes. such as large aerial foragers and aquatic special. bird-like non-avian theropod dinosaurs. (A) The four-winged dromaeosaurid Microraptor gui (photo by Mick Ellison). not surprisingly this the toes). (C) The large short-armed dromaeosaurid Zhenyuanlong suni (photo by Junchang Lu¨). Patagopteryx. flight- primitive avifauna exhibited less ecological diversity than mod. 2015 ª2015 Elsevier Ltd All rights reserved . although there ists [34]. These basal ornithurines are restricted ern assemblages. and demonstrates that many major lin. teeth in both jaws and the absence of a hypotarsus (a structure with representatives of every major early avian group present of the ankle in living birds that guides the pulley-like tendons of [33]. is some fossil evidence for Cretaceous species [38]. and Apsaravis. kin). which grade on the line to Ornithurae. larger generalists are present. in terms of both numbers of fossils and taxonomic diversity (50 named species). These are the oldest unequivocally avian fos. The single best record of a Creta- eages were already well established in the Early Cretaceous ceous neornithine is the partial skeleton of Vegavis from the lat- [35]. These so-called ‘oppo- site birds’. tenuous taxonomic affinity. Among these skeletons [31. a group of large. (Sapeornis and kin).37]. Current Biology Review Figure 2. but certain extant ecomorphs True modern birds — members of the crown group Neo- were absent. China. Small arborealists.32]. a derived subgroup that includes have yielded thousands of almost complete and fully articulated modern birds and their closest fossil relatives. a gull-like species with nearly sils after Archaeopteryx and account for approximately half of modern avian skeletal features except for the retention of large the total recorded global diversity of Mesozoic bird species. These latter birds include Sapeornithiformes the well-developed hypotarsus [39]. example fossils in Figure 5).7–120 million years ago) Jehol Biota of Liaoning Province. whose members are characterized by several modifications to the flight apparatus that probably made them more powerful and efficient fliers. narrow furcula (wishbone). lived which is assigned to the subgroup of modern birds including alongside the earliest birds with a pygostyle (a fused. October 5. Montage of feathered. dated be.7 and 120 million years ago. Sinornithosaurus (photo by Mick Ellison). which form a tween approximately 130. The long bony-tailed Jeholornithiformes (Jeholornis and est Cretaceous (around 68–66 million years ago) of Antarctica. such as the fossils of the Jehol Biota of northeastern China. These latter two groups together form the derived clade Ornithothoraces. All specimens from the Early Cretaceous (130. R888–R898. less diving birds [30. evolving into a and Sinornis and were distributed worldwide during the Creta- number of groups of varying anatomy and ecology [30] (Figure 1. R890 Current Biology 25. This evi- The Jehol biota provides a spectacular window into the dence mostly consists of extremely fragmentary specimens of early evolution of birds. and the earliest members of the major early bird groups Enantior- nithes and Ornithuromorpha [33]. Yixianornis. Gansus. named because they differ from modern birds in the construction of the shoulder girdle (ornithuromorphs Mesozoic Birds: The First 100 Million Years of Avian have a concave scapular cotyla. whereas this surface is History convex in enantiornithines). rnithes — are a mostly post-Cretaceous radiation. The enantiornithines were the dominant group of Cretaceous birds. This diversification is recorded by Ornithuromorphs include a slew of Cretaceous birds. only slightly more derived than Archaeopteryx. and reduced hand [30]. Although highly diverse for its time. reduced ducks and geese (Anseriformes) based on the morphology of tail bone).

but all basically indistinguishable from the flight feathers of living birds depictions are remarkably bird-like. hair-like fila- bird-like appearance of derived non-avian dinosaurs close to the common ments called ‘protofeathers’ that are widely considered to be ancestor of birds. another function. or perhaps even in the closest relatives of dinosaurs [48. This suggests that their initial purpose was not for flight. times. which are used to construct an airfoil for flight (the wing). sexual selection may have been the initial driving force in the vians closely related to birds [3. evolved.51]. Liaoning. tor. Middle-Late Jurassic. [48]. are now known from Reconstructed.44]. and the bizarre ‘crouched’ hindlimb posture. are absent in the earliest birds and evolved. Over the past two decades of research. dinosaurian relatives.e. Behaviors and only later were they co-opted into flight structures in the The ever-growing fossil record of early birds and their closest earliest birds and their very closest dinosaurian relatives. tions other than flight. Some non-bird dinosaurs like Microraptor possess feathers with various degrees of reptilian and avian features reconstructed. vaned feathers are family tree (Figure 1). Whether these wings were capable inated. branching. A variety of primitive theropods. such as the keeled breastbone to support flight muscles for flight coming later [35]. 2015 ª2015 Elsevier Ltd All rights reserved R891 . it is the only taxon with asymmetrical hindlimb feathers (flight what we think of as the bird ‘blueprint’ was pieced together grad. hinge-like The evolution of feathers likely began in the earliest dinosaurs.B). artistic and scientifically informed appearance of a small troodontid dinosaur and its surrounding environment. feathers. early birds in which a sternum is present (Jeholornis. raptor suggests that it was a capable glider. This small body size is a culmination Other non-bird dinosaurs may have used their wings for func- of an evolutionary trend spanning more than 50 million years. The envi. but fingered hands of birds first appeared in primitive theropods. The male (left) is shown displaying to the female. and ornithothoracines) [62]. the legs and tails [55–59]. likely for display and/or thermoregulation. one ing or display [60]. such as rapid growth.19. The story of feather evolution is becoming increasingly clear: the earliest feathers evolved in The Assembly of the Bird Body Plan and Classic Avian non-flying dinosaurs. allow unprecedented insight into how the layered together to form wings on the arms. and perhaps even flight — Some non-bird dinosaurs probably did use their wings to fly. although probably tures. is difficult to answer at present. in which the femur is held nearly horizontal and most of the locomotory activity of the hindlimb oc- curs at the knee joint rather than the pelvic joint [47]. suggesting that the ability to fold the forearm against the body evolved in para. Tianyulong and Kulindadromeus [50.20]. and a growing number of plant-eating ornithischian dinosaurs. and one fell swoop (Figure 1) [2. such as Sinosaur- opteryx and the tyrannosaurs Dilong and Yutyrannus [17]. Although hindlimb feathers are often beginning in maniraptoran theropods distantly related to birds regarded as evidence that birds evolved flight through a four- [40–42]. wing stage [58]. illustrating the incredibly spectacularly preserved fossils covered in simple. Therefore. which became wings in birds ([45]. meaning that the earliest birds looked more like dinosaurs in lacking these features. a feature of all of this ‘blueprint’ below. [53–55] (Figures 2 and 3). although there overarching pattern has become clear: many features — such as is some emerging evidence for multiple uses. evolution of complex paravian plumages. and egg brooding. often multiple birds [61]. pygostyle. Illustration by Jason Brougham (http://jasonbrougham. Confuciu- Living birds are mostly small and have a highly distinct skel. Long-term trends in skeletal proportions and muscula- ture across dinosaurs and early birds led to two of the most char- acteristic features of living birds: the elongated arms. hollowed bones. such as display [63]. with their use as airfoils tures. Other artistic illustrations and feathers of modern birds occurred in maniraptoran theropods interpretations for these advanced paravian dinosaurs exist in the literature. and not capable of the kind of muscle-driven powered flight of living beak. wishbones. A troodontid dinosaur. Perhaps the single most recognizable feature of birds is feathers. The bipedal posture. Other classic avian fea. egg brooding..20]. October 5. such as Figure 3. vaned seasonally dry woodland dominated by bennettites and cycads. and also for display. one of the closest relatives to birds. a majority of tail the reversion of the pubis and associated forward movement morphologies of early birds and close dinosaurian relatives of the center of mass occurred in maniraptoran theropods.19. a keeled sternum. Other fea. China) is a these structures into the more complex.Current Biology Review and highly reduced tail. these feathers are symmetrical (i. In further support of Microraptor’s volant capabilities. evolved after the origin of birds. which can be placed in a well-resolved In many derived non-bird dinosaurs. sornis. not well and long S-shaped neck of birds were inherited from deep dino. and appear to be primarily ornamental in function. or perhaps used for other functions. that are seen only in birds among living animals first evolved in Biomechanical study of the four-winged dromaeosaurid Micro- the dinosaurian ancestors of birds (Figures 4 and 5). eton well suited for flight. A display function for many of these Current Biology 25.49] (Figure 4A. constructed for flight) in all known species other than Microrap- saurian ancestors [43. R888–R898.52]. not during and are optimized to withstand the force of the airstream). but see [46]). and in some cases classic body plan and signature behavioral features of birds orig. We describe the assembly the only non-avian with an elongated coracoid. and were related to the phenomenal success of of flight. the wishbone (furcula) and three. the earliest stage of feather evolution [48. Similarly. Elaboration of ronment (Tiaojishan Formation. in more derived birds during the Cretaceous.3. thermoregulation. such as egg brood- the group (Figure 4). feathers are asymmetrical with a short and stiff leading vane ually over many tens of millions of years of evolution.

but a sternal keel was apparently lacking in powered flight as we know it in modern birds most certainly the most basal members. all other photos by Mick Ellison. (C) Parent oviraptorosaur brooding its nest of large eggs. near the origin of Ornithuromorpha. yellow. The slightly more derived Jeholornis keen senses. Montage of bird-like features in non-avian theropod dinosaurs. muscles. ities that varied substantially between groups. (F. telencephalon. but had several derived evolution [72] and non-bird paravians had the highly expanded. green. although early resemble ornithuromorphs in many anatomical features of the birds and even some non-bird dinosaurs had volant capabilities. a narrow excavated furcula with a short hypocleidium. red. a tail reduced to a fused plough-shaped pygostyle. it of kilometers [1].I) by Amy Balanoff. vaned feathers forming a wing on the arms of the dromaeosaurid Zhenyuanlong suni. enabled by a keeled sternum supporting enormous flight evolved flightworthy plumage of large wings composed of asym. sacral vertebrae. the pulley-like system that automates the upstroke). thus caused the feathers to have a diversity of colors [64]. R888–R898. enabled in part by a forebrain that is expanded possessed a curious mixture of features: it retained a primitive relative to body size [71]. (I) The brain of the modern woodpecker Melaner- pes. Current Biology Review Figure 4. (A) Simple filament-like ‘protofeathers’ on the head of the compsognathid Sinosauropteryx. we hold that the following is most likely. These inno- This latter hypothesis is bolstered by the recent realization that vations then combined with features evolved earlier in birds and flight probably evolved multiple times within maniraptoran dino. which al- gliding flight through the use of fleshy patagia similar to flying lows some species to fly at altitudes of 9. R892 Current Biology 25. a complex sternum. Second.000 meters (such squirrels [29]. olfactory bulb. an elongated coracoid with a procoracoid process (important in creating the pulley-like system used to minimize effort in the upstroke. much of the evolution of complex It was only in birds much more derived than Archaeopteryx feathers and wings in paravian dinosaurs was driven by factors and Jeholornis that the fully modern style of avian flight devel- other than flight. enabled by structures other than feathered wings: the ered forelimbs and a narrow furcula. present evidence.G) Pneumatic foramina (de- noted by arrows). (D) Furcula (wishbone) of the dro- maeosaurid Bambiraptor feinbergorum. Enantiornithines strongly worthy feathered wings in parallel as well. midbrain. relating like modern birds. hindbrain). and probably had primitive flight capabil. (H) The re- constructed brain of the troodontid Zanabazar ju- nior (orange. 2015 ª2015 Elsevier Ltd All rights reserved . flight-related features of modern birds. where air sacs penetrated the bones. First. un. brain of early birds [73] (Figure 4). in a cervical vertebra (F) and rib (G) of the tyrannosaurid Alioramus altai. some paravians that oped. such as elongation of the feath- saurs. have had a triosseal canal [69]. (B) Large. muscle-driven flight seen in today’s birds. branching. only a single basal taxon appears to developed after the origin of birds themselves. If derived bird-like dinosaurs were experimenting as some vultures and geese) and over distances of hundreds with using different body structures to evolve flight in parallel. Living birds are highly intelligent with large flight muscles [62. which would have lift and allowed the long tail to be used as a stabilizer. flight apparatus. images in (H. otherwise only present in the Ornithuromorpha). their non-dinosaurian relatives. Photo in (B) by Junchang Lu¨. based on flight [68]. Jeholornis also had its own peculiarities: it possessed a complex feathers would also explain demonstrated increases in unique fan-shaped tract of tail flight feathers that likely increased melanosome diversity in these dinosaurs.65]. and a curved scapula [66.67]. This expansion began early in theropod long. October 5. For example. Third. This modern style of flight developed with or follows that different dinosaurs may have evolved different flight. (E) Hollow internal cavity in the tibia of the tyrannosaurid Alioramus altai. bony tail unlike that of extant birds. such as display. blue. Other distinctive anatomical features of modern birds. the flight feathers on the tail (retrices) in modern birds [70]. first evolved in their even a compensatory specialized gastral basket for anchoring dinosaurian ancestors. and their robust pygostyle ap- The earliest birds lacked many key features related to powered pears to have been unable to support the muscles that control flight in modern birds. cerebellum. metrical feathers (such as Microraptor and perhaps other taxa and a complete triosseal canal in the shoulder (which encloses that await discovery) evolved flight in parallel to flight in birds. such as numerous fused and presumably ‘flight ready’. to produce the style of high- enigmatic maniraptoran clade Scansoriopterygidae also evolved ly efficient. producing its own unique and probably very effective form of Therefore. Archaeopteryx lacked a bony sternum and to the sensory and respiratory systems.

93]. All specimens from the Early Creta- ceous (130.95]. As tree (Figure 1). but more gradually over a hatchling to adult within a few weeks or months.13]. non-bird dinosaurs [83]. is that most dino. such as Archaeopteryx. China. (Figure 4F. October 5. What is certain. Determining the physiology of dino.82]. birds had its roots in the mesothermic physiologies of dinosaurs. and sequential ovulation were acquired in maniraptoran Recent work has surprisingly shown that this system first began dinosaurs closely related to birds [87.84]. there was a huge spike in rates of saurs grew much faster than previously realized. and the amplified rates and rapid matu- ration of modern birds probably evolved somewhere around the Birds Dealt with a Crisis at the End of the Cretaceous origin of Ornithurae [3. at a rate inter. associated with high rates of hindlimb evolution and greater such as enantiornithines. such that only a single oocyte (or none) is ovu- lated. Egg size progressively increased and and elaborate during the course of theropod evolution [77–80] clutch size decreased during early avian evolution [90]. The acid rain. shelled.7–120 million years ago) Jehol Biota of Liaoning Province. intermediate be. and which is linked to a complex sys. triggered a global cataclysm of climate and temperature change. (B) The enantiorni- thine Eopengornis martini. which had so-called ‘mesothermic’ physiologies. Later. The course of avian history was dramatically affected by the saurs is difficult and has been the source of considerable debate mass extinction at the end of the Cretaceous. smaller tem of balloon-like air sacs that store air outside of the lungs [74]. non-bird dino. derived near- to evolve in reptiles. The air sacs evolved in early dinosaurs. The reproductive system of living birds is remarkably derived compared to their closest living relatives (crocodilians) and other vertebrates. The extinction was geologically rapid and most reptiles [85]. clutches. However. ago. earthquakes. which typically are actively brooded in the nest by one which oxygen passes across the gas exchange tissues during or both parents [1] (Figure 4). A recent comprehensive study found that dinosaurs likely caused by the impact of a large asteroid or comet. usually maturing from in one or a few spurts of innovation. behavioral features of birds (the bird ‘blueprint’) did not evolve Extant birds grow remarkably fast. anatomical evolution in the earliest birds [2]. perhaps related to body lightening during the into vertebrae and other bones. (A) The basal avian Sapeornis chaoyangensis (ju- venile.G). there apparently were some bursts of shown by studies of bone histology and growth curves based evolution in the early history of birds. as ovary. however. tally: derived microstructural eggshell characteristics. 66 million years for decades [11. (C) The basal avian Jeholornis prima. which wiped out all non-avian dinosaurs and many other saurs had high metabolisms more similar to birds than to living groups [92. but was ab- sent in basal birds and developed later in avian history. They lay small clutches of large. therefore possessed a ‘bird-like’ lung. asymmetrical eggs formed by two or three crystal Modern birds also possess an efficient ‘flow through’ lung in layers. Birds possess only a single functional ovary and oviduct and have oocytes that mature rapidly. The lution of short-tailed birds (Pygostylia) in the Cretaceous was oldest birds. R888–R898. and This summary illustrates how the classic anatomical and possibly other dinosaurs. and Mesozoic bird groups. Once a small flight-capable on counting lines of arrested growth in bones. indicating that the left ovary was lost very close to the dino- shown by the distinctive foramina where the air sacs penetrate saur–bird transition. as extant crocodiles and monitor lizards bird dinosaurs apparently retained two functional ovaries [89]. and have a long period of evolutionary time and across the dinosaur family high-powered endothermic (‘warm-blooded’) metabolism. the early evo- mediate between that of reptiles and modern birds [81.88].76]. tsunamis. photo by Huali Chang). Montage of Mesozoic birds. and laid per 24-hour cycle (not numerous eggs en masse as in croc- odilians and many dinosaurs). exhibit unidirectional breathing [75. Photos in (B–D) by Jingmai O’Connor. It is emerging consensus is that the endothermic physiology of living possible that somewhat longer-term changes in the Earth Current Biology 25. and wildfires [94. These features evolved incremen- inhalation and exhalation. 2015 ª2015 Elsevier Ltd All rights reserved R893 .Current Biology Review Figure 5. (D) The basal ornithuromorph Iteravis huchzermeyeri. However. had growth rates similar to derived than normal speciation [91]. dinosaur had been assembled. and became more extensive evolution of flight [90]. but without a complex whereas Jeholornis and enantiornithines apparently had a single system of air sacs. Most theropod dinosaurs at the very least. tween ‘cold-blooded’ ectotherms and endotherms [86].

2015 ª2015 Elsevier Ltd All rights reserved . such as enantiornithines cates that nearly all modern ordinal lineages formed within 15 and basal ornithuromorphs) living alongside what was probably million years after the extinction [4]. leaving Current Biology them the only surviving members of the initial Mesozoic radiation of birds. countering the ste- Columbea Pterocliformes (Sandgrouse) Columbi- NEOGNATHAE morphae reotype that the mass extinction deci- Columbiformes (Doves) mated the non-avian dinosaurs but largely Phoenicopteriformes (Flamingos) Phoenicopteri. suggesting a particularly a moderate diversity of early neornithines. Australaves Passeri. Current Biology Review Passeriformes (Oscines) Figure 6. however. Coracii- Trogoniformes (Trogons) morphae Text color denotes groups of species with broadly Afroaves shared traits. Pelecaniformes (Cormorants) Procellariiformes (Fulmars) Procellarii- 91 Sphenisciformes (Penguins) morphae Gaviiformes (Loons) Gavii- 70 morphae Phaethontiformes (Tropicbirds) Phaethonti- Eurypygiformes (Sunbittern) morphae enantiornithines and basal ornithuro- Charadriiformes (Plovers) Cursori. including volcanism and sea-level fluctuations. and shows that these birds diversified rapidly in the post-apoc- ture. divergence time in millions of years. Numerous groups space. because of the scrappy fossil record Anseriformes (Waterfowl) of the latest Cretaceous birds. Fossil system. with many of the record during the 10 million years after the end-Cretaceous characteristic lineages of ‘archaic’ birds from the Jehol Biota (spe. as indicated by rare rapid period of both genetic evolution and the formation of new fossils and molecular phylogenetic studies tracing some modern species (Figure 6). and the very bird-like non-avian dinosaurs. introns. This also indicates that birds 55 Musophagiformes (Turacos) Otidi.000 species of birds living in today’s world are den. spared birds (see reviews in [92. release afforded by the extinction of both the ‘archaic’ birds ing other organisms an opportunity to radiate in the vacant eco. probably taking advantage of the ecological the Cretaceous. None of these ‘archaic’ further below. may [100. The dashed line represents the approximate Accipitri- Accipitriformes (New World Vultures) morphae end time (50 million years ago) by which nearly all Passerea 96 neoavian orders diverged.97. The arrow at the bottom indicates the 84 Coliiformes (Mousebirds) Cretaceous–Paleogene boundary at 66 million Strigiformes (Owls) years ago. Ordinal-level genome-scale family Vocal learners Passeriformes (Suboscines) tree of modern birds.99]). of modern neornithines make their first appearance in the fossil Birds were diverse in the Late Cretaceous. apparently survived past the Cretaceous and into the Paleogene. whether by homology or conver- Leptosomiformes (Cuckoo-roller) gence. Names on Coraciiformes (Bee-eaters) branches denote orders (-iformes) and English Piciformes (Woodpeckers) group terms (in parentheses). with many major early Cuculiformes (Cuckoos) Mesitornithiformes (Mesites) groups going extinct. R888–R898. The emerging pic. There has long been debate Birds after the Cretaceous about whether the extinction of ‘archaic’ birds was gradual or sud. To the right are su- 72 Bucerotiformes (Hornbills) perorder (-imorphae) and higher unranked names. How- Podicipediformes (Grebes) morphae Galliformes (Landfowl) ever. with the Cretaceous period shaded at Accipitriformes (Eagles) left. however. non-neornithine birds. but recent evidence shows that a diverse avifauna of divided into two major groups: the Palaeognathae (which R894 Current Biology 25. morphs persisted until at least a few hun- 96 Gruiformes (Cranes) morphae dred thousand years before the end of 91 Opisthocomiformes (Hoatzin) the Cretaceous in western North America. Horizontal gray bars on Core waterbirds (Aequornithia) Pelecaniformes (Pelicans) Pelecaniformes (Herons) each node indicate the 95% credible interval of Pelecani. is that the world changed suddenly at the end of alyptic world. killing off many once-dominant groups and giv. Figure used Pelecaniformes (Ibises) morphae and modified with permission from [4]. Caprimulgiformes (Hummingbirds) suggesting that the extinction was sudden Caprimulgiformes (Swifts) Caprimulgi- Caprimulgiformes (Nightjars) morphae and directly linked to the end-Cretaceous NEOAVES 91 Otidiformes (Bustards) impact [99]. Core landbirds (Telluraves) Psittaciformes (Parrots) and ultraconserved elements. All bootstrap Cariamiformes (Seriemas) values are 100% except where noted. Branch colors Falconiformes (Falcons) represent well-supported clades.101] and recent genetic [4] evidence supports this view have also played a role in the extinction [96]. it PALAEOGNATHAE Struthioniformes (Ostrich) has been unclear why certain birds went Cretaceous Paleogene extinct and others survived. October 5.39. were strongly affected by the end-Creta- morphae ceous extinction. and a genome-scale molecular phylogeny indi- cies outside of the neornithine crown.98]. The tree was generated from 30 million base Birds of prey Passeriformes (New Zealand Wrens) morphae Waterbirds pairs of genomic DNA consisting of exons. extinction [102]. 110 100 90 80 70 60 50 40 30 20 10 0 Multiple lineages of early neornithines Millions of years ago must have endured the extinction. which is GALLOANSERES Tinamiformes (Tinamous) mostly limited to isolated bones [99]. We discuss this recent phylogenomic study lineages into the Cretaceous [4. The more than 10.

parrots. This is a very rare trait. As such. waterbird orders) were found to be sister clades [107] and their The phylogenetic relationships of Neoaves have been the sub. The main in the regions of the brain that control song (bird) and speech (hu- differences with some previous molecular studies are that man) [98. grebes. and determine that the majority of tors in North and South America during much of the Cenozoic these groups diverged immediately after the Chicxulub asteroid (around 62–2 million years ago) [107. Among the sequence (using up to 300 million nucleotides) and number ‘core’ waterbird group. beginning with the sunbittern/tropicbird clade the general branching patterns between the major orders on and culminating in penguins and pelicans amongst others. seen in only in songbirds. and mesites (Figure 6). chickens. October 5. avian vocal learners have become highly studied occurred within the first 15 million years after the mass animal models of human speech [110–112].104] and the hypothesis that shorebird-type by two subsequent losses in New Zealand wrens and subo- species were able to endure the extinction [100. The recent phylogenomic of pigeons. that the aquatic or terrestrial adaptations of these groups with scale analysis of birds to date in terms of amount of DNA the ‘core’ waterbirds and landbirds are convergent. evolution in parrots and songbirds (Figure 6) [4]. [4] is the most comprehensive genome. and attempted to resolve two main issues: firstly.108]. these findings reveal the great amount of the Jarvis et al. including tionships among well-known living birds. on the branch leading to Passerimorphae (parrots to We predict that this ancestor may have been ecologically similar songbirds) (Figure 6). 2015 ª2015 Elsevier Ltd All rights reserved R895 .106]. All three However. However. such as kiwis. but within this group the rapto- mon ancestor of Neoaves lived in the Cretaceous. the new phylogenomic study supports Cretaceous revolution.97. nearly all of these ordinal divergences mates. The subsequent burst of specia. closely related to the extinct giant terror resolve. on the branch leading to Coraciimorphae lumbea (consisting of doves. the new analysis supports two independent gains of vocal In general. with the highest level of certainty to date.Current Biology Review includes flightless forms.g. which the bird family tree. and humans) but not non-human pri- As mentioned above. One interpretation of such inde- gnathae split. [4] study are consis. which help to better un- ducks. and secondly. [4]. although more evi- Columbea and Passerea split. seriemas/falcons) are predatory.105. to obtain an aquatic or semi-aquatic versus terres. dence is needed to confirm this. over time. particularly which groups originated before the end-Cretaceous The common ancestor of the ‘core’ landbirds was inferred to extinction and which arose afterwards. there appears to be a graded acquisition of analyses. (mousebirds to bee eaters). these new results are at odds with previous molec. The names of Afroaves and Australaves to modern shorebirds. The new phylogeny also helps to better understand the evolu- tion after the extinction consisted of an initial rapid radiation of tion of one of the most intriguing traits of some living birds: vocal additional basal Neoaves orders. followed diation of birds [99. elephants. and thereby also after the Neo. pelicans. of aquatic traits. and geese) and Neoaves (which includes derstand the evolution of important anatomical and ecological everything from pigeons and owls to falcons and parrots) traits. dolphins. (including penguins. R888–R898. learning. since the number of divergences after the imply their likely geographical origins [109]. bats. it does not completely rule out independent that may have allowed them to live in diverse environments. deepest branches of ‘core’ landbirds (vultures/eagles/owls and According to the dated phylogeny of Jarvis et al. Afroaves clade. the remainder of bird diversity. (including birds of prey. in turn. the com. sandgrouse. Overall. parrots. The species at the impact that ushered out the Cretaceous. but Modern birds achieved their enormous diversity over a more the key interval of speciation and ordinal-level diversification than 150 million year evolutionary journey. and sand.98. Among the Columbea. the flamingos and grebes (both [4.101] with traits scines. In sum. [100]). is The new phylogenetic analysis revealed some surprising rela- composed of the subgroup Galloanserae (the ‘fowls’.103] (Figure 6).110. which began with their Current Biology 25. and loons) and ‘core landbirds’ and hummingbirds among birds and very few mammals (e. years ago. flamingoes. The earliest rial trait appears to have been lost twice: once among the divergence of this ancestor gave rise to the major subgroups Co. vocal-learning bird lineages and humans were found to have ular studies suggesting a major pre-Cretaceous divergence of evolved convergent mutations and changes in gene expression Neoaves 20–100 million years earlier [97. in which some of the main extant lineages originated during Conclusions the final few tens of millions of years of the Cretaceous.113]. In contrast to long- extinction. emus. [4] study used genomic-scale data and took diversity and convergence that occurred among birds (including a conservative approach of using non-ambiguous fossils for some features convergent with mammals) during the post- dating the tree. This suggests study by Jarvis et al. the speciose clade that includes ceous extinction. The Neognathae.g. closest relatives were inferred to be a landbird group consisting ject of extensive work in recent years. and was concentrated in the few million years after the end-Creta- rheas) and the Neognathae. birds (Phorusrhacidae) that included human-sized apex preda- lationships of modern birds. and again among the Australaves grouse) and Passerea (consisting of all other neoavian species). once in the common ancestor of parrots and songbirds. Another interpretation is that this trait was passively nathae and Galloanseres are predicted to have passed through lost twice. the ordinal re. and songbirds). woodpeckers. At least four to six of costly lifestyle for modern birds and is being selected against these basal Neoaves lineages and several members of Palaeog. with this pulse of evolution ending around 50 million standing inferences of three independent gains [103. are more obligate water-dwellers. including the ability of some species to imitate human followed by two subsequent radiations of ‘core waterbirds’ speech.114]. when these groups diverged. pendent losses of the raptorial trait is that being a predator is a trial species are almost equal (Figure 6) [4]. ostriches. from grebes to hummingbirds. learning amongst Neoaves: once in the hummingbirds and tent with earlier studies proposing a major post-Cretaceous ra. The study was able to be an apex predator. the results of the Jarvis et al. a ‘short fuse’ hypothesis for modern bird diversity (e. clade. the end-Cretaceous extinction.

(2013a). Cal. 153. P.. Benson. O’Connor. an Early Cretaceous terrestrial La- Solenhofen. Z. Sci. M. P. G.A. Ji.. (2011).M. Warnow. Escuillie´. Mindell.. Chiappe. 1320–1331. F. (Berkeley: Univ. of California Press). Li.H. Z. pp. 277–299. Commun.-L. C. 2. H. and Zanno. Witmer. (2012). J. S. Mus.L. and Makovicky.E. Nat. A. Soc. Zhang. and Zhen. Nat.. Ho.. S. 889–906. theropod from China.. and Zhou. Kaiser. 147–152. Soc. Ornithology. Nabholz. Aberer.a synop- tic review. Owen. A. (2003).A. Y. London 26. Larsson.-H. B. (2011). 1253293. and HHMI support to E. X. (1863).B. 24. 4... R. J. O. and G. and Xu. (2002). The Jehol Biota. M. 31. continued with the gradual 14.B. P.. NJ: Wiley-Black- Museum of Natural History to S. M.. Makovicky. A. J. Rev.. Trans. Dong-Yu. 81–85. The flurry of recent work on avian evolution is a prime example of how fossil. R. NJ: Wiley). from the lithographic stone of 32.J. Bakker.J. S. T. G.M. Norell.-M. 9–29. Wenhao..-T. 24. and E. (1998). F.A. 6. and G. and L. in dinosaurs. and Zhou. Z. S.. beishanensis (Aves) and a comprehensive phylogeny of Mesozoic birds.. J. and X. O’Connor. Turner. reveals some greater truths about evolution over long time. Wang. Z. Erickson. Huxley.B. Barrett. 2nd edition (Berkeley: Univ. and G. Company). Am.. P.J. H. Dromaeosauridae. P. 1–206. M.J.. J.. J. Zhou. and Makovicky. (2014).. 35. Escuillie´. Padian.. Gilbert...M. Skeletal morphology and sys- tematics of the Cretaceous Euenantiornithes (Ornithothoraces: Enatior- 13. Sci. theropod from China and the origin of Avialae. Dyke. 2015 ª2015 Elsevier Ltd All rights reserved . 70–73. (2013b). 465–470. phylogenetic. and Walker. 66–75. C. X. Vertebr. Mackem. 2. Ostrom. Biol. G. 25. Houde. Nat. eds. B.M. J. X. Cau..T. Sci. Low ecological disparity in Early Cretaceous Birds. Nat. 33–47. Gradual G.T. avian divergences in the Mesozoic..K. C. 34. Further evidence of the affinity between the dinosau- rian reptiles and birds. and Novas. (2014).L. Peabody Mus.. and Ji. and H. Weishampel. Hist. F. G. L. (2012). Acad. In Living Dinosaurs.J. C. G.H. Wang. pp. Zhou. 1. eds. S.. Gill.Y. Rev.. Biol. An exceptionally well-preserved theropod dinosaur from the Yixian Formation of China. An integrative approach to understanding bird origins. Z. In Mesozoic Birds: Above the Heads of Dinosaurs. Dong. Z.M. and 17. 1–17. Ann. and Norell.K. Xu. M. The Dinosaur Heresies (New York: William Morrow). Mitchell.-M.C. Zhang. Biol. with a description of Lower Cretaceous ecosystem. Anatomical and ecological evidence of endothermy nithes)... Comm. Dyke. the fossil remains of a long-tailed species.J. R. and piecemeal acquisition of a flight-worthy body plan. Bakker. Zheng. (2004). and Rauhut. Turner. X. Li. and Osmo´lska. The oldest record of Ornithur- omorpha reveals heterogeneous rates of morphological evolution among 12. of California Press).. On the Archeopteryx of von Meyer. Chen. 1394.T. Dinosaur Paleobiology (Hoboken. (2007). Z. L.. Agnolı´n. P. A.J. X. T. 20140608.T. 7.A. Makovicky. (1986).. Marie Curie Career Integration Grant EC 630652. F. J. S. H. H.. winged dinosaur was fully assembled. S.T. Faircloth.K. P.. D. (2006). R. G..L. R. G. H. A review of dro- maeosaurid systematics and paravian phylogeny. Osteology of Deinonychus antirrhopus. Prum.W. Tischlinger. refinement of avian characteristics..J. Xu. 11. An Archaeopteryx-like 3.D. un- derwent long and often unpredictable paths of evolution. Mirarab. F. 281. L. Q. morphological. Wang. 543–559. Makovicky. theropod from the Lower Cretaceous of Montana. Hist. (1926). Proc. B.M. 240–267. (1972)... G. and Norell.. Theropod diversity and the cies became so successful. and Bell. 359–362. F. New specimen of Archaeopteryx provides insights into the evolution of pennaceous REFERENCES feathers. Geol.. 196–209.. Mirarab. Wang. This work is funded by NSF DEB 1110357.-L. Gauthier.C. Fjeldsa. On the discovery of the earliest bird fossil in China when a small. Chuong. 26. Xu for discussions with sauria. Du. Kaier. (2002). (1986). an NSF GRF.-H. P. P. and ence 346. Columbia University. (Hoboken. Zheng. A. 1–55. 19. 8. Zhou. et al. Houde. K. and second when surviving species had the freedom to thrive af- ter the end-Cretaceous extinction. Nature 511. Phil. (Berkeley: Univ. 2386–2392. 73. (1969). R896 Current Biology 25. Brusatte. 33. Nat. D. 79–82. L.. Zhang for discussions with E. Dyke. Sci. Dodson. Heilmann.K. Sci.. R. Lloyd. 371... Palasiat. Rev. X. and the American 22. eds. (1996). (1868). Godefroit. Avian Ancestors (Heidelberg: 1. and statis. 28. Foth.D. Zhou. Why ornithologists should care about the theropod origin of birds.. Curr. Lloyd. A bizarre Jurassic maniraptoran theropod with pre- served evidence of membranous wings. You. F.. eds.. M. Dececchi.B.. D.O. D. (1870). October 5. and involved two bursts of diversification: first in the Mesozoic 15.H. 18. J. (2013).L. (2015).D.M. Nature 391. (2011)..P.. Brusatte. Norell.. Quar. 12–31. Lloyd. W. 27. S.. Mag. On the animals which are most nearly intermediate between birds and reptiles. Chiappe. K. Dodson. X. pp. J. D. Palaeontol. (2004). ACKNOWLEDGMENTS 21. The Dinosauria. Saurischian monophyly and the origin of birds. S. 20.. 33. (2014). the dinosaur-bird transition.A. The Origin of Birds (London: Witherby). Chinese Geology 10. feathered. A. Current Biology Review divergence from theropod dinosaurs. 9. and Dyke. Feathered dinosaurs. Xu.L.) and the origin of birds. Nature 521.H. A Jurassic avialan dinosaur from China resolves the early assembly of avian body plan culminated in rapid rates of evolution across phylogenetic history of birds. birds. A redescription of Chaoyangia Sons). (1998). Nature 421. Choiniere. Wiley & 6. Wang. Wang. Howard. R. J. Sullivan. S.. namely that major living groups have a deep history.. M. Nature 475. O’Connor. 3rd edition (London: W. Dyke..E. T. were given unexpected opportunities to radiate if they were able to survive mass extinctions that decimated other groups.. M. 10. J. P. Mesozoic birds of China . Lee. Nat. Pre-modern birds: Hist. (2013).. Jarvis. 1–42. The origin of avian diversity 16. P. Huxley. and Han.. S. scales. In Living Dinosaurs: the Evolutionary History of Birds. Bull. C. 36. The origin and early evolution of tical data can be combined to weave an evolutionary narrative. Cracraft. Hu.. G. 74–98. 1–165. (2014). and Varricchio. O’Connor. and Claeys.M. 29. F.-C. genomic. nov.D.T..B. pp. Freeman and Springer Briefs in Earth System Sciences). gersta¨tte: new discoveries and implications. Braun. 2nd edition.S. (2015).A. Godefroit.. In The Dino- P. P. Weishampel.-C. H. 30. X. S. Dudley. (Sinosauropteryx gen. R888–R898. and Zhang. Whole-genome analyses resolve early branches in the tree of life of modern birds. We thank well). 39–114. (2005). and Chiappe. Demuynck. 23.-H. Osmo´lska... An exceptionally preserved 7. 6987. Lond.H. Nature 498. Norell. Earth Plan. Bull. Reduced plumage and flight ability of a new Jurassic paravian 4.. (2014). 8. P. J. 30–33. L. and Hilton. (New Jersey: J. Mem.. 5. and explain how some of the modern world’s most familiar spe. Science 346. J. 807–814. Syst.. E. (2014). Chiappe. 44.-T. The Auk 119. Nature 238.L. of California Press). Ho. X. 30. an unusual Early Cretaceous birds.. Annu.

T. You. R888–R898.S. 45. Proc. R. 93. Longrich. X.. Zhou.I. Soc. S.. Basic avian pulmonary dontid theropod from China with long feathers on the metatarsus. Anat. Ji. short-armed.E. 20. 71.J. 305–308.. H. J...-M. Zhao. L.. J.R..-T... Q. and Zhou. Zhou.. Zhou. higher-level phylogeny of Archosauria (Tetrapoda: Diapsida).K. (1993)..Current Biology Review 37. R. S. M. Nature 501.. 1955–1959. Sci. L. Commun. J.. The early evolution of archosaurs: relationships and (Paraves) and Sapeornis (Aves) and the complex early evolution of the the origin of major clades. and Ga- napathisubramani. 133–152. Nature 393.N. and Xu. Zheng. 1378–1381.M.. and Sanders.M. M.. 104–107. J.. R. Martinez..-H. and Xu. D. L. and L. F.M. evolution indicate 170 million years of sustained ecological innovation on the avian stem lineage. 339–388. L. T.. Mannion.S. Desojo.P.. Zhang. Paleontol.L.. eds. ‘Mod. H. new predatory dinosaur from Argentina.. Carrano.. and Wang. Norell. (2013). and Guo. Four.. Butler. Wang.. X. and Chiappe.A. Rowe. M. Wang. J. 3–47.A. K. Pol.. C. Science 345.. Vertebr Palasiat.. D. Lu¨. C. F..M. An Early Creta. (1998).V. and Sander.K. (2010). O’Connor. R. Meng. Wilson.L. Zhang. (2014). 53.A. J. and Zhang. C. 76. Definitive fossil evidence for the extant avian radiation in the Cretaceous. McNamara. Norell. Q. Exp. Evolu- ischian dinosaur from Siberia with both feathers and scales. P. Q. Development and evolutionary origin of feathers. 367–370. The origin and early radiation of dinosaurs.. Wang. and Evans.. Tubaro.C. 335–340. Mus. J. rainbow. (2015).M.. Hindlimb feathers in paravians: primarily ‘wings’ or ornaments? Zoolog. Emb. (2013). 70. L.. V. S..B. Chiappe. Northcutt.-M. its implications for feather evolution.M. (1971). D... and Claessens. Science 4.J. 149–187. Beyond the 39.. Sci. 47.. Current Biology 25.. 1–292. G. J. (Berkeley: University of California Press).A. Unique caudal plumage of Jeholornis and complex saurs. L. R.O. Sci. and Norell. J. J. USA 111. X. winged dromaeo- 38. (2003). R. P. Bates. compared. Aerodynamic performance of the feathered 40. 45.. G. J. (2015).G..doi. 2489.-L. (1999).E. Sereno.M.-T.. Dececchi. Zhang. J. pp. Z. M. O’Connor. 61. Li. USA 110. (2014). F.. X. Evidence for avian intrathoracic air sacs in a Anchiornis huxleyi... 311–329. 22. 285.. Clarke. G. and Zhou. Brusatte. (2000). and Ketcham. Kuang. Brusatte. Unidi- 54. Sinitsa. A pre-Archaeopteryx troo. F.R. 220–225.K. (2009). 753–761. Gao. 451–455.A. Theropod forelimb design and 66. Ji.. (2014). 48. The origin and early evolution of feathers: in- 69... Benton. J.T. Paleontol. 50. X. M. 65. Zheng.. Nature 421. e3303. 34. Sullivan. evolution. 55. 416–418. P.. A Jurassic ornith. and Zhou. Z. (2013).. and Hutchinson. Rev. M. Biol. A. Koschowitz. Farmer. R. O’Connor. Zhou. Q. Sereno. Sullivan.G. Nature 426. M. X. T.D..A. F. Wang. Linn. tica 47. Wang. Xu. Bull. Na- ern’ feathers on a non-avian dinosaur. (2011).. Nature design and flow-through ventilation in non-avian theropod dinosaurs.1036141. Linking the evo- 68. P. (2011). M. and Shawkey. Lee. 5. lution of body shape and locomotor biomechanics in bird-line archo- and Zhou. Nat. 46. The gastral basket in basal birds and their close relatives: size and C.A. saurs from northeastern China.. Syst.. D’Alba.. Alcober.J.-F... Duncker. Evolving large and complex brains. Pneumatic postcranial bones in dinosaurs and other ar- winged dinosaurs from China. A basal dromaeosaurid and size evolution preceding avian flight. 317. 1–171. J. 333– 43. Clarke. Benton.-J.R. 8..K. A. Two feathered dino. Z. M. Cell Biol. Nat.P.. PalAsia- origin of feathers. 51. (2013). and Wilson. Zhang.A.R.C. Melanosome evolution indicates a key physiological shift within feathered dinosaurs. Cretaceous Hesperornithiformes (Aves: Ornithuromorpha): implications Wang. 77. Bolotsky. 41. ceous heterodontosaurid dinosaur with filamentous integumentary structures. Dhouailly.. (2000).-L. X. Li. 640–643.C. A large.J. (2009). P. K. rectional pulmonary airflow patterns in the savannah monitor lizard. Science 327. J. (2014). E. Noriega. (2013). and Gatesy. Yuan. (2008).. Allen. Nature 507. C. Proc. Clarke. R. Li. O’Connor. A species-level phylogeny of the 58. (2014).G. Z. and Spagna. 11775. 338–340. 36–37. 60. G. (2007). Balanoff. C. Naish. dinosaur Microraptor and the evolution of feathered flight. Hind wings in basal for body size evolution amongst the earliest diving birds. X. Z. D. (2010). N. J. D. and avian flight from a new clade of Early Cretaceous ornithurines from China Norell.Y. Zhang.. (2006).. and Du. Earliest stages in the evolution of ation at the origin of birds: uncoupling allometric constraints across a the modern avian skeleton: Archaeopteryx and the Jehol avifauna macroevolutionary transition. Rep. Wang. Am. H.. PhD thesis (University of Calgary). Acad. M. tionary origins of the avian brain. (2013).... avian sternum. Campione. K. Currie. Middleton.A.D. van der Kindere. 72.-H. J.. Gao. P. N. Science 290. Q. and Chang. (2000). Zhou.. 2262–2267. Acad. Zool. G. In Mesozoic saurid (Dinosauria: Theropoda) from the Early Cretaceous of China and Birds: Above the Heads of Dinosaurs.M.-Q. 57.-C. Zhang.. J.B.E.-C. S.. 287–308.A. 68–100.E. 12.M. Evolution 67. Science 346. Z.-H. M.T.. M. Li. O’Connor.1080/14772019. Prum.. Naturwissen- schaften 90. 1309–1312. Cau. Erickson.L. X. 352.. (2002).. Y. Nature 416. K.K. 208.. 461.-M.J. Witmer. J.. A. The Mesozoic radiation of Neornithes.. with a new understanding of the earliest avian evolution.-L. Cieri..-T. Syst. (2002). Z.J. X..J.A. and Russell. S. X. Y. Nat.. Tambussi. 2015 ª2015 Elsevier Ltd All rights reserved R897 ... P. Z. 93–96.. Hope. Palmer. Q. and Brusatte. and Zhang. The lung air sac system of birds.J. X.-H. Dyke. J. J.. A. (2012). Rates of dinosaur body mass possible function.L.. 74.P. Godefroit. of alligators. 62. Palae. Hist. J.P. Sizov. D.. H. P. D.. Adv. Zool. (2014). X. (2003)..H. Fischer. D. R. 73. and Ji. Zhang. C. Varricchio.M. Zheng. and Norell. X. Y. Britt. (2014). 63. 1166–1172. Turner.. 562–566. and Dyke. ture 506. 42. Vinther..A. PLoS Biol. Erickson. A primitive enantiornithine bird and the sights from recent paleontological and neontological data. Irmis. Nesbitt.. H.2015. Nat.. Schachner. chosaurs. X. 291–306. On the absence of sternal elements in Anchiornis 44. 101.E.. Sci... X. 59. e1001853.. Z.J. October 5. Anat. M.. G. Wang.. C.. ontol. Upchurch.L.. tail evolution in early birds. 17404–17408. A. B.M... (2014). Butler.. Jeholornis compared to Archaeopteryx. Wei. Zheng.J. Primitive wing feather arrangement in Archaeopteryx lithographica and and Larsson. Science 339. Science 332. Xu. M. (2015). S. M. (2005).A. Nature 497. (2014). 128. A. Y. Xu. J. 2741–2752. B. de Kat. J.C... (2009). Unidirectional airflow in the lungs 53. S. 253–256. birds. Nature 433.A. S. Bell.B. X... birds and the evolution of leg feathers. 79. Z.. Hou.C. and Larsson.L. (2010). Body and limb size dissoci- 67...A. 52. O. X.C. Sustained minia- turization and anatomical innovation in the dinosaurian ancestors of 64. Science 345. Vert. Hu. Zheng. Nature 458. X. X. 75. Naish. L. Pa- laeontol.... and Dong. X. Bever. Clarke. Earth and the morphology of Yixianornis grabaui. Insight into the evolution of 49. Zhang. H. J. Larsson.. (2005). S. Vert. http://dx. 615–618.. K. J. Meng.. Curr.. Forebrain enlargement among theropod dinosaurs.-L. S. 197A. M. and Langer.. Z. Benson. and Zhou. P. PLoS One 3. 78. 13900–13905. 926–927. Benton.. Nesbitt.B. The 350–353. Vert. 56.M.B. O’Connor. C. and Farmer.

R. Science 346. A pair of shelled eggs inside a female dinosaur..A. A. 91.. Soc. 2nd edition. Wang. X.J. O. C.L. (1997)...R. 87. Mass extinction of birds? Reconciling slow growth in Archaeopteryx. Science 103. Rates of dinosaur limb evolu- tion provide evidence for exceptional radiation in Mesozoic birds..R.. et al. Res. M. 6. Meredith. F. F. Howard. sity Press).L. O. Sci. J. R. P. 154. and J. A.. Schulte. Borkowski. Flying rocks and flying tion of avian reproductive traits.I. X... Science 208. and Mooers.R. In The Dinosau.E.C. Roulhac. Antunes. Cockell.J. 94. I..-T. and L. et al. Evol. Dinosaur physiology.. (2004). Bralower. Exploring the Evolution of Mind and Brain (Cambridge. (Bloomington: Indiana Univer.K.B.A. Phillips. et al. 4.V. R. 101. P. Cret. birds at the Cretaceous-Paleogene (K-Pg) boundary. Rogers.. L.D. pelhus. (2004). 95.A. Carrano. (2004). E. Zool. C.. M. and Jarvis.C. 100. T. 90.. USA 108. tions and the ‘reptile’-bird transition.H. G. F. II. Sci- 83. (2014). Benson. pp. K. G. 1311–1320. D. 1016. Forey. J. P.J. Extraterres. Thomas. Ksepka. (2012). Lond. Philos. mans and song-learning birds. Butler. M. MacLeod.J. Explosive evolution in Tertiary birds and mammals. G. Alvarenga. S. Claeys. J. 1268–1272. Nature 412. Y. (2015).V. Jarvis. Pratt. biogeography and parallel radiations..T. 637–683. (1997).. J. 85. Ganapathy. Evans. C. 81. J. B. Current Biology Review 80. (2001). Norell.. B. and Field. BoudagherFadel.. and Ho¨fling... Nature 412. Dettweiler-Robinson. (Berkeley: Univ. P. (2014). In The Air-filled postcranial bones in theropod dinosaurs: physiological implica. P. PLoS One 4. G. L. P. Mayr. Science 267. J. Jetz. Sci. 1095– M.T. (2012). W.M. Speech. Dodson. A.J. and H. Biogeog.. Bone microstructure of early birds. de Ricqle`s. 55–91.C. Li. Greenwold.N.. MA: MIT Press). Feduccia. G. pp.D. and Hsiao. The extinction of the dinosaurs.A. Erickson. Biol..B. Evol. Witmer. Dinosaurian growth rates 98. Y. Tokaryk. Wright.. Proc. Petkov.A. (2009). 112. and Language: Camb. G.. Mayr. 140. Z.. Alvarez. 109. T. 185–214....T. Joy.J.R. N. Butler. Proc. R. Erickson.M. A.D. C. and Michel. (2001). In Feathered Dragons: 104. M. Grady. 96. D. Hara. Varricchio. R. 106. A. and Horner.L. D.C. Alvarez.. Nat. D.. A.W.R. (2010). sessing the magnitude and subsequent explosive radiation.T. Hu. Bown. Turner. Kop. 172–176. 2nd edition. trial cause for the Cretaceous-Tertiary extinction. Nature 495. G. 1–15. Nature 385. 247–250..-H. Asaro.. and Norell.T.V. 102. Chinsamy. 97. Bolhuis. ‘Big Bang’ for Tertiary birds? Trends Ecol. Science 327.. D. 114. Papeis Avulsos de Zoologia 43. Storz.. eds.-C.C. Carrano. Rauhut. G. Gibb. Barton..M. and Lamm. 149. Soc. 265–292. G. J. Soc. P.L.J. Geol.B. Wu. 628–642. Q.. E. and Fastovsky. (2009). 157–169. Zool. signal enhancement. J. P. Osmo´lska.. J. Arz. Christeson. Zheng.. (2004). Zhou.. (2007). P.J.. J. 50. Learned birdsong and the neurobiology of human lan- M.. (2014).. Barrett.. 2015 ª2015 Elsevier Ltd All rights reserved . Arenillas. eds. and Smith. E. Sato. (2003). Hendy..F. of California Press). P. Weishampel.A.M.. Was dinosaurian physiology inherited by 99. Analysis and discussion. Brusatte. 313–326.M. 108.A. BMC Biol. Mol. Philos. M. Erickson. birds (Theropoda. K. ria. R. D. D. and Penny. E. Biol. data. Dinosaur extinction.. Bown. 444–448.M. 20131780. Larkin.. R.. J. A. Padian.J. 87.L. Linn. and spoken lan- guage origins: behavioral phenotypes and neurobiological substrates. Longrich. Evol. (Berkeley: Univ. Pfenning. Alegret.H. Feduccia. e7390.. P.L.G.S.-N. The Chicxulub asteroid impact and mass extinction at the Cretaceous. Birds.. In Mesozoic Birds: Above the Heads of Dinosaurs. 672–684.... October 5. 88. Mannion. pp. Dinosaurian growth (2012). 18.J. Banner. J.. B.M. (2013)..M.. Currie. and Williamson. Osmo´lska. clocks: disparity in fossil and molecular dates for birds.. Zelenitsky. L.. 749–777. R898 Current Biology 25. M.. 375.F. NY Acad. (1995). K. A. J. J. Nature 491. Rev.J. 39. Padian. Wang. Sci. Livezey. Soc.A..F.. (Berkeley: Univ.. and Zusi.D. 105. (2003). Strong mitochondrial DNA support for a Cretaceous origin of modern avian lineages. 113.W. Comparative geno- mics reveals insights into avian genome evolution and adaptation. F. (2008). (2013). and Yerby. W. Aves: Neornithes) based on comparative anatomy.. Higher-order phylogeny of modern 344. Ann. (2014). and bird origins. Systematic revision of the 507–511.. D. Wirthlin. Enquist. P. Proc. primates.R. S..J. 1214–1218.. Evolution of terrestrial birds in three continents: Biol. M. J. 813–824... Neurosci.D... Feduccia. Brown. G. Chang. 92. (2004). P. R. (2014).J. F.. Morphological evidence for sister group relationship be- tween flamingos (Aves: Phoenicopteridae) and grebes (Podicipedidae). R888–R898..W. D..E. (2012). 421–431. Weishampel. Wang. K.-L. Li. Preservation of ovarian follicles re- veals early evolution of avian reproductive behaviour. Ware. E.. eds. 280. Lovell.. guage. ence 346.B. Birdsong. Benson. Huchzermeyer. Z. Rev. G.. M.W.. and H. Acad.. P. and Everaert.. M. 107. 15253–15257..M. 405–408.. (2002). 1256846. Lee. 429–433. Wright. Whitney.J.L. 20140677. 168–193.A... X. and priors. 89..K. The global diversity of birds in space and time. Toward resolving deep Neoaves phylogeny: 1108. Wang. 660–671. and Horner.D. L. Biol. Peppe. and Choiniere. (2012).O. Front. Sci.B. P. Dinosaur eggs and nesting: implications for understanding the origin of birds... M. P. O’Connor. Dinosauria. 111. T. 12. otic transition. H. J. J. 281.W. (2013). Rivas. 1–95. Jackson. Paleogene Fossil Birds (Berlin: Springer). Evidence for mesothermy in dinosaurs.. N. T.. Archibald. and Chiappe. Lloyd. 82. Convergent transcriptional specializations in the brains of hu- Paleogene boundary. The Cretaceous-Tertiary bi. 26.. 84... Zhang.S. 110. Morgan-Richards. Li. Camb. P. Nest and egg clutches of the dinosaur Troodon formosus and the evolu. N. (2009)...T. Soc. Phorusrhacidae (Aves: Ralliformes). Avian extinction at the end of the Cretaceous: as- Studies on the Transition from Dinosaurs to Birds. H. pp. (2005). Upchurch.. Hartmann. Linn. Chiappe. Inouye. 86. B.. D. and Horner. and Zhou.J.-F. of California Press). M. Science 308. patterns and rapid avian growth rates. and Burnett. Dodson. E. Rawson. 6. D. Y.. eds... and O’Connor. of California Press). R. K. 90.B. M. D. 93. (1980). J. J. Grellet-Tinner.M. Shugar. J. Biol.