Birds are one of the most recognizable and diverse groups of modern vertebrates. Over the past two decades, 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 dinosaurs 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

Birds are one of the most conspicuous groups of animals in the modern world. They are hugely diverse, with more than 10,000 extant species distributed across the globe, filling a range of ecological niches and ranging in size from the tiny bee hummingbird (∼2 grams) to the ostrich (∼140,000 grams). Their feathered bodies are optimized for flight, their supercharged growth rates and metabolism stand out among living animals, and their large brains, keen senses, and the abilities of many species to imitate vocalizations and use tools make them some of the most intelligent organisms on the planet [1].This begs a fascinating question: how did birds achieve such great diversity and evolutionary success? For much of the last two centuries this was a mystery, but over the past two decades a wealth of new fossil discoveries, molecular phylogenetic analyses of living birds, and quantitative macroevolutionary analyses have revolutionized our understanding of bird origins and evolution. This new information reveals a surprising story: birds evolved from dinosaurs and have a deep evolutionary history, during which their signature body plan evolved piecemeal over ∼100 million years of steady evolution alongside their dinosaurian forebears before many of the modern groups of birds explosively diversified after the non-avian dinosaurs went extinct 66 million years ago (Figure 1) (e.g. [234]).

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Figure 1Summary phylogeny (genealogical tree) of birds. The phylogeny shows where birds fit into the larger vertebrate family tree and the relationships of the earliest birds and their closest dinosaurian relatives (based on [2]
 and other studies cited therein). Timescale values are in millions of years; thick red line denotes the mass extinction at the Cretaceous–Paleogene boundary caused by asteroid impact (denoted by fireball on the right); arrows denote lineages that survived the extinction; circles represent species known from a particular point in time; thick line sections of branches indicate direct fossil evidence and thin lines are temporal distributions implied by phylogenetic ghost lineages; Cz, Cenozoic interval after the end-Cretaceous extinction. Silhouette anatomical features in the lower part of the figure are plotted approximately where they evolve on the phylogeny. Species silhouettes at the top of the image are from phylopic.org and designed by (from left to right): Nobu Tamura, Anne Claire Fabre, T. Michael Keesey, Steven Traver, Andrew A. Farke, Mathew Wedel, Stephen O’Connor/T. Michael Keesey, Brad McFeeters/T. Michael Keesey, Scott Hartman, T. Michael Keesey, Scott Hartman, Scott Hartman, Matt Martyniuk, Matt Martyniuk, Matt Martyniuk, Matt Martyniuk, Nobu Tamura/T. Michael Keesey, Matt Martyniuk, J.J. Harrison/T. Michael Keesey. ‘Bipedal posture’ silhouette by Scott Hartman.

The origin of birds is now one of the best understood major transitions in the history of life. It has emerged as a model case for using a combination of data from fossils, living species, genealogies, and numerical analyses to study how entirely new body plans and behaviors originate, and how prominent living groups achieved their diversity over hundreds of millions of years of evolution [23]. Here, we review what is currently known about the origin, early diversification, and rise to dominance of birds, and the various lines of evidence that piece together this story.Note that throughout this review, we use the vernacular term ‘birds’ to refer to a specific group, which is defined in a phylogenetic sense as the most inclusive clade containing Passer domesticus (the house sparrow) but not the extinct bird-like dinosaurs Dromaeosaurus albertensis or Troodon formosus. This clade includes all living birds and extinct taxa, such as Archaeopteryx and Enantiornithes. Some researchers refer to this group as Avialae (e.g. [25]), but others use the name Aves (e.g. [6]). In this review, we avoid these debates by referring to this group as ‘Avialae/Aves’ and its members as ‘avians’. We use Neornithes to refer to the avian crown group, which comprises all living birds and the descendants from their most recent common ancestor.

 The Dinosaur–Bird Link: Once Controversial, Now Mainstream

What did birds evolve from and where do they fit into the family tree of life? For much of the 19th and 20th centuries these questions were hotly debated. The first hint that birds evolved from reptiles appeared in 1861, only a few years after Darwin published On the Origin of Species, with the discovery of an exquisite skeleton of a Late Jurassic (ca. 150 million year old) bird from Germany. Named Archaeopteryx by British anatomist Richard Owen, this fossil possessed a curious mixture of classic bird features, such as feathers and wings, but also retained sharp claws on the hands, a long bony tail, and other reptilian characteristics [7]. Over the next two decades, Thomas Henry Huxley — Owen’s great rival and Darwin’s most vociferous early supporter — argued that Archaeopteryx bore remarkable similarities to small dinosaurs like Compsognathus, supporting an evolutionary link between the groups [89]. This idea gained some acceptance, but fell out of favor during the early 20thcentury, largely as a result of an influential book by Danish anatomist Gerhard Heilmann [10]. Up until the 1960s most scientists held that birds originated from a nebulous ancestral stock of reptiles called ‘thecodonts’.The debate over bird origins was reinvigorated in the 1960s–1980s, as a new generation of paleontologists spearheaded the ‘Dinosaur Renaissance’ [11]. John Ostrom discovered fossils of the astonishingly bird-like dinosaur Deinonychus in western North America [12], Robert Bakker and colleagues argued that dinosaurs grew fast and had active metabolisms like living birds [13], and Jacques Gauthier and colleagues used the revolutionary new technique of cladistics to place birds within the family tree of dinosaurs [14]. By the 1990s the vast majority of paleontologists accepted the dinosaur–bird link, but many ornithologists remained skeptical. The discovery in the late 1990s in China of fossils from thousands of bona fide dinosaurs covered in feathers provided the most definitive visual evidence for the dinosaur–bird link [151617], convincing most of the remaining skeptics (Figure 2A–C). It is now widely accepted, even by ornithologists, that birds evolved from dinosaurs [18], with the two groups linked by hundreds of shared features of the skeleton, soft tissues, growth, reproduction, and behavior [2319202122]. Most amazingly, it is now known that many non-bird dinosaurs were feathered and would have looked much more like birds than lizards or crocodiles (Figure 3).

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Figure 2Montage of feathered, bird-like non-avian theropod dinosaurs. (A) The four-winged dromaeosaurid Microraptor gui (photo by Mick Ellison). (B) The small long-armed dromaeosaurid cf. Sinornithosaurus (photo by Mick Ellison). (C) The large short-armed dromaeosaurid Zhenyuanlong suni (photo by Junchang Lü). All specimens from the Early Cretaceous (130.7–120 million years ago) Jehol Biota of Liaoning Province, China.
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Figure 3A troodontid dinosaur, one of the closest relatives to birds. Reconstructed, artistic and scientifically informed appearance of a small troodontid dinosaur and its surrounding environment, illustrating the incredibly bird-like appearance of derived non-avian dinosaurs close to the common ancestor of birds. The male (left) is shown displaying to the female. The environment (Tiaojishan Formation, Middle-Late Jurassic, Liaoning, China) is a seasonally dry woodland dominated by bennettites and cycads. Illustration by Jason Brougham (http://jasonbrougham.com/). Other artistic illustrations and interpretations for these advanced paravian dinosaurs exist in the literature, with various degrees of reptilian and avian features reconstructed, but all depictions are remarkably bird-like.

Where Birds Nest in the Dinosaur Family Tree

Birds evolved from dinosaurs, and therefore are dinosaurs, in the same way that humans are a type of mammal (Figure 1). Birds are nested within the theropod dinosaurs, the major subgroup of mostly carnivorous species that includes the behemoths Tyrannosaurus and Allosaurus, but also smaller and obviously much more bird-like species such as VelociraptorDeinonychus, and Troodon [2122]. Birds are members of a nested set of ever-more exclusive theropod subgroups: Coelurosauria, Maniraptora, and Paraves (Figure 1). Their very closest relatives are the mostly small-bodied, feathered, large-brained dromaeosaurids and troodontids, exemplified by the well-known Velociraptor [23].However, the exact relationships among paravians (birds, dromaeosaurids, and troodontids) are uncertain and often vary between competing phylogenetic analyses based on morphological characters, because as more fossils are found it is becoming clear that the earliest birds were very similar anatomically to primitive dromaeosaurids and troodontids, so it is difficult to tell them apart. Thus, there is current debate about whether dromaeosaurids and troodontids form their own clade of close bird relatives, or whether one of them is more closely related to birds than the other [2524]. This means that there is also ongoing debate about which fossils are the earliest birds. The iconic Archaeopteryx is still widely considered to be among the first birds [25242526], but some studies have suggested that it may instead be a primitive dromaeosaurid or troodontid [2728]. Additional studies have also found other small feathered theropods, such as Anchiornis and Xiaotingia, to be the earliest birds [2426], more primitive than Archaeopteryx. There is also debate about whether the bizarre, sparrow-to-pigeon-sized, long-fingered scansoriopterygids are basal-most birds or non-bird maniraptorans [2524252629].These debates will likely continue, but the alternative answers do not change two important points: firstly, that birds first appear in the fossil record during the Middle–Late Jurassic, around 165–150 million years ago (the age of ArchaeopteryxXiaotingiaAnchiornis, and close dromaeosaurid and troodontid relatives); and secondly, that the oldest birds and their closest relatives were small (roughly chicken-sized), lightweight, long-armed, winged, and feathered animals (Figure 4A,B). The fact that scientists are having a difficult time distinguishing the earliest birds from their closest dinosaur relatives illustrates just how bird-like some non-bird dinosaurs were (Figure 3), and how the transition between non-bird dinosaurs and birds was gradual.

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Figure 4Montage of bird-like features in non-avian theropod dinosaurs. (A) Simple filament-like ‘protofeathers’ on the head of the compsognathid Sinosauropteryx. (B) Large, branching, vaned feathers forming a wing on the arms of the dromaeosaurid Zhenyuanlong suni. (C) Parent oviraptorosaur brooding its nest of large eggs. (D) Furcula (wishbone) of the dromaeosaurid Bambiraptor feinbergorum. (E) Hollow internal cavity in the tibia of the tyrannosaurid Alioramus altai. (F,G) Pneumatic foramina (denoted by arrows), where air sacs penetrated the bones, in a cervical vertebra (F) and rib (G) of the tyrannosaurid Alioramus altai. (H) The reconstructed brain of the troodontid Zanabazar junior (orange, olfactory bulb; green, telencephalon; blue, cerebellum; red, midbrain; yellow, hindbrain). (I) The brain of the modern woodpecker Melanerpes. Photo in (B) by Junchang Lü; images in (H,I) by Amy Balanoff; all other photos by Mick Ellison.

 Mesozoic Birds: The First ∼100 Million Years of Avian History

Birds had diversified by the Early Cretaceous, evolving into a number of groups of varying anatomy and ecology [30] (Figure 1; example fossils in Figure 5). This diversification is recorded by the fossils of the Jehol Biota of northeastern China, dated between approximately 130.7 and 120 million years ago, which have yielded thousands of almost complete and fully articulated skeletons [3132]. These are the oldest unequivocally avian fossils after Archaeopteryx and account for approximately half of the total recorded global diversity of Mesozoic bird species, with representatives of every major early avian group present [33]. Although highly diverse for its time, not surprisingly this primitive avifauna exhibited less ecological diversity than modern assemblages. Small arborealists, semiaquatic taxa, and larger generalists are present, but certain extant ecomorphs were absent, such as large aerial foragers and aquatic specialists [34].

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Figure 5Montage of Mesozoic birds. (A) The basal avian Sapeornis chaoyangensis (juvenile, photo by Huali Chang). (B) The enantiornithine Eopengornis martini. (C) The basal avian Jeholornis prima. (D) The basal ornithuromorph Iteravis huchzermeyeri. Photos in (B–D) by Jingmai O’Connor. All specimens from the Early Cretaceous (130.7–120 million years ago) Jehol Biota of Liaoning Province, China.

The Jehol biota provides a spectacular window into the early evolution of birds, and demonstrates that many major lineages were already well established in the Early Cretaceous [35]. The long bony-tailed Jeholornithiformes (Jeholornis and kin), only slightly more derived than Archaeopteryx, lived alongside the earliest birds with a pygostyle (a fused, reduced tail bone). These latter birds include Sapeornithiformes (Sapeornis and kin), the beaked Confuciusornithiformes (a clade of early birds including the abundantly found Confuciusornis), and the earliest members of the major early bird groups Enantiornithes and Ornithuromorpha [33]. These latter two groups together form the derived clade Ornithothoraces, whose members are characterized by several modifications to the flight apparatus that probably made them more powerful and efficient fliers, such as a keeled sternum (breastbone), elongate coracoid, narrow furcula (wishbone), and reduced hand [30]. The enantiornithines were the dominant group of Cretaceous birds, in terms of both numbers of fossils and taxonomic diversity (∼50 named species). These so-called ‘opposite birds’, named because they differ from modern birds in the construction of the shoulder girdle (ornithuromorphs have a concave scapular cotyla, whereas this surface is convex in enantiornithines), include such taxa as Gobipteryx and Sinornis and were distributed worldwide during the Cretaceous [36].Ornithuromorphs include a slew of Cretaceous birds, such as GansusPatagopteryxYixianornis, and Apsaravis, which form a grade on the line to Ornithurae, a derived subgroup that includes modern birds and their closest fossil relatives. Among these close relatives are Ichthyornis, a gull-like species with nearly modern avian skeletal features except for the retention of large teeth in both jaws and the absence of a hypotarsus (a structure of the ankle in living birds that guides the pulley-like tendons of the toes), and the Hesperornithiformes, a group of large, flightless diving birds [3037]. These basal ornithurines are restricted to the Late Cretaceous.True modern birds — members of the crown group Neornithes — are a mostly post-Cretaceous radiation, although there is some fossil evidence for Cretaceous species [38]. This evidence mostly consists of extremely fragmentary specimens of tenuous taxonomic affinity. The single best record of a Cretaceous neornithine is the partial skeleton of Vegavis from the latest Cretaceous (around 68–66 million years ago) of Antarctica, which is assigned to the subgroup of modern birds including ducks and geese (Anseriformes) based on the morphology of the well-developed hypotarsus [39].

 The Assembly of the Bird Body Plan and Classic Avian Behaviors

The ever-growing fossil record of early birds and their closest dinosaurian relatives, which can be placed in a well-resolved family tree (Figure 1), allow unprecedented insight into how the classic body plan and signature behavioral features of birds originated, evolved, and were related to the phenomenal success of the group (Figure 4). Over the past two decades of research, one overarching pattern has become clear: many features — such as feathers, wishbones, egg brooding, and perhaps even flight — that are seen only in birds among living animals first evolved in the dinosaurian ancestors of birds (Figures 4 and 5). Other features, such as rapid growth, a keeled sternum, pygostyle, and beak, are absent in the earliest birds and evolved, often multiple times, in more derived birds during the Cretaceous. Therefore, what we think of as the bird ‘blueprint’ was pieced together gradually over many tens of millions of years of evolution, not during one fell swoop (Figure 1) [231920]. We describe the assembly of this ‘blueprint’ below.Living birds are mostly small and have a highly distinct skeleton well suited for flight. This small body size is a culmination of an evolutionary trend spanning more than 50 million years, beginning in maniraptoran theropods distantly related to birds [404142]. The bipedal posture, hinge-like ankle, hollowed bones, and long S-shaped neck of birds were inherited from deep dinosaurian ancestors [4344], the wishbone (furcula) and three-fingered hands of birds first appeared in primitive theropods, the reversion of the pubis and associated forward movement of the center of mass occurred in maniraptoran theropods, and the ability to fold the forearm against the body evolved in paravians closely related to birds [31920]. Other classic avian features, such as the keeled breastbone to support flight muscles and highly reduced tail, evolved after the origin of birds, meaning that the earliest birds looked more like dinosaurs in lacking these features. Long-term trends in skeletal proportions and musculature across dinosaurs and early birds led to two of the most characteristic features of living birds: the elongated arms, which became wings in birds ([45], but see [46]); and the bizarre ‘crouched’ hindlimb posture, in which the femur is held nearly horizontal and most of the locomotory activity of the hindlimb occurs at the knee joint rather than the pelvic joint [47].Perhaps the single most recognizable feature of birds is feathers, which are used to construct an airfoil for flight (the wing), and also for display, thermoregulation, and egg brooding. The evolution of feathers likely began in the earliest dinosaurs, or perhaps even in the closest relatives of dinosaurs [4849] (Figure 4A,B). A variety of primitive theropods, such as Sinosauropteryx and the tyrannosaurs Dilong and Yutyrannus[17], and a growing number of plant-eating ornithischian dinosaurs, such as Tianyulong and Kulindadromeus [5051], are now known from spectacularly preserved fossils covered in simple, hair-like filaments called ‘protofeathers’ that are widely considered to be the earliest stage of feather evolution [4852]. Elaboration of these structures into the more complex, branching, vaned feathers of modern birds occurred in maniraptoran theropods [48]. Some non-bird dinosaurs like Microraptor possess feathers basically indistinguishable from the flight feathers of living birds [535455] (Figures 2 and 3). The story of feather evolution is becoming increasingly clear: the earliest feathers evolved in non-flying dinosaurs, likely for display and/or thermoregulation, and only later were they co-opted into flight structures in the earliest birds and their very closest dinosaurian relatives.In many derived non-bird dinosaurs, vaned feathers are layered together to form wings on the arms, and in some cases the legs and tails [5556575859]. Whether these wings were capable of flight, or perhaps used for other functions, such as egg brooding or display [60], is difficult to answer at present, although there is some emerging evidence for multiple uses.Some non-bird dinosaurs probably did use their wings to fly. Biomechanical study of the four-winged dromaeosaurid Microraptor suggests that it was a capable glider, although probably not capable of the kind of muscle-driven powered flight of living birds [61]. In further support of Microraptor’s volant capabilities, it is the only taxon with asymmetrical hindlimb feathers (flight feathers are asymmetrical with a short and stiff leading vane and are optimized to withstand the force of the airstream), and the only non-avian with an elongated coracoid, a feature of all early birds in which a sternum is present (JeholornisConfuciusornis, and ornithothoracines) [62].Other non-bird dinosaurs may have used their wings for functions other than flight. Although hindlimb feathers are often regarded as evidence that birds evolved flight through a four-wing stage [58], these feathers are symmetrical (i.e., not well constructed for flight) in all known species other than Microraptor. This suggests that their initial purpose was not for flight, but another function, such as display [63]. Similarly, a majority of tail morphologies of early birds and close dinosaurian relatives appear to be primarily ornamental in function, suggesting that sexual selection may have been the initial driving force in the evolution of complex paravian plumages, with their use as airfoils for flight coming later [35]. A display function for many of these complex feathers would also explain demonstrated increases in melanosome diversity in these dinosaurs, which would have caused the feathers to have a diversity of colors [64].Therefore, we hold that the following is most likely, based on present evidence. First, much of the evolution of complex feathers and wings in paravian dinosaurs was driven by factors other than flight, such as display. Second, some paravians that evolved flightworthy plumage of large wings composed of asymmetrical feathers (such as Microraptor and perhaps other taxa that await discovery) evolved flight in parallel to flight in birds. This latter hypothesis is bolstered by the recent realization that flight probably evolved multiple times within maniraptoran dinosaurs, enabled by structures other than feathered wings: the enigmatic maniraptoran clade Scansoriopterygidae also evolved gliding flight through the use of fleshy patagia similar to flying squirrels [29]. If derived bird-like dinosaurs were experimenting with using different body structures to evolve flight in parallel, it follows that different dinosaurs may have evolved different flightworthy feathered wings in parallel as well. Third, although early birds and even some non-bird dinosaurs had volant capabilities, powered flight as we know it in modern birds most certainly developed after the origin of birds themselves.The earliest birds lacked many key features related to powered flight in modern birds, and probably had primitive flight capabilities that varied substantially between groups. For example, unlike modern birds, Archaeopteryx lacked a bony sternum and even a compensatory specialized gastral basket for anchoring large flight muscles [6265]. The slightly more derived Jeholornis possessed a curious mixture of features: it retained a primitive long, bony tail unlike that of extant birds, but had several derived flight-related features of modern birds, such as numerous fused sacral vertebrae, an elongated coracoid with a procoracoid process (important in creating the pulley-like system used to minimize effort in the upstroke, otherwise only present in the Ornithuromorpha), a complex sternum, a narrow excavated furcula with a short hypocleidium, and a curved scapula [6667]. Jeholornis also had its own peculiarities: it possessed a unique fan-shaped tract of tail flight feathers that likely increased lift and allowed the long tail to be used as a stabilizer, thus producing its own unique and probably very effective form of flight [68].It was only in birds much more derived than Archaeopteryx and Jeholornis that the fully modern style of avian flight developed, enabled by a keeled sternum supporting enormous flight muscles, a tail reduced to a fused plough-shaped pygostyle, and a complete triosseal canal in the shoulder (which encloses the pulley-like system that automates the upstroke). These innovations then combined with features evolved earlier in birds and their non-dinosaurian relatives, such as elongation of the feathered forelimbs and a narrow furcula, to produce the style of highly efficient, muscle-driven flight seen in today’s birds, which allows some species to fly at altitudes of ∼9,000 meters (such as some vultures and geese) and over distances of hundreds of kilometers [1]. This modern style of flight developed with or near the origin of Ornithuromorpha. Enantiornithines strongly resemble ornithuromorphs in many anatomical features of the flight apparatus, but a sternal keel was apparently lacking in the most basal members, only a single basal taxon appears to have had a triosseal canal [69], and their robust pygostyle appears to have been unable to support the muscles that control the flight feathers on the tail (retrices) in modern birds [70].Other distinctive anatomical features of modern birds, relating to the sensory and respiratory systems, first evolved in their dinosaurian ancestors. Living birds are highly intelligent with keen senses, enabled in part by a forebrain that is expanded relative to body size [71]. This expansion began early in theropod evolution [72] and non-bird paravians had the highly expanded, and presumably ‘flight ready’, brain of early birds [73] (Figure 4). Modern birds also possess an efficient ‘flow through’ lung in which oxygen passes across the gas exchange tissues during inhalation and exhalation, and which is linked to a complex system of balloon-like air sacs that store air outside of the lungs [74]. Recent work has surprisingly shown that this system first began to evolve in reptiles, as extant crocodiles and monitor lizards exhibit unidirectional breathing [7576], but without a complex system of air sacs. The air sacs evolved in early dinosaurs, as shown by the distinctive foramina where the air sacs penetrate into vertebrae and other bones, and became more extensive and elaborate during the course of theropod evolution [77787980] (Figure 4F,G). Most theropod dinosaurs at the very least, and possibly other dinosaurs, therefore possessed a ‘bird-like’ lung.Extant birds grow remarkably fast, usually maturing from hatchling to adult within a few weeks or months, and have a high-powered endothermic (‘warm-blooded’) metabolism. As shown by studies of bone histology and growth curves based on counting lines of arrested growth in bones, non-bird dinosaurs grew much faster than previously realized, at a rate intermediate between that of reptiles and modern birds [8182]. The oldest birds, such as Archaeopteryx, and Mesozoic bird groups, such as enantiornithines, had growth rates similar to derived non-bird dinosaurs [83], and the amplified rates and rapid maturation of modern birds probably evolved somewhere around the origin of Ornithurae [384]. Determining the physiology of dinosaurs is difficult and has been the source of considerable debate for decades [1113]. What is certain, however, is that most dinosaurs had high metabolisms more similar to birds than to living reptiles [85]. A recent comprehensive study found that dinosaurs had so-called ‘mesothermic’ physiologies, intermediate between ‘cold-blooded’ ectotherms and endotherms [86]. The emerging consensus is that the endothermic physiology of living birds had its roots in the mesothermic physiologies of dinosaurs, but was absent in basal birds and developed later in avian history.The reproductive system of living birds is remarkably derived compared to their closest living relatives (crocodilians) and other vertebrates. Birds possess only a single functional ovary and oviduct and have oocytes that mature rapidly, such that only a single oocyte (or none) is ovulated, shelled, and laid per 24-hour cycle (not numerous eggs en masse as in crocodilians and many dinosaurs). They lay small clutches of large, asymmetrical eggs formed by two or three crystal layers, which typically are actively brooded in the nest by one or both parents [1] (Figure 4). These features evolved incrementally: derived microstructural eggshell characteristics, smaller clutches, and sequential ovulation were acquired in maniraptoran dinosaurs closely related to birds [8788]. However, derived near-bird dinosaurs apparently retained two functional ovaries [89], whereas Jeholornis and enantiornithines apparently had a single ovary, indicating that the left ovary was lost very close to the dinosaur–bird transition, perhaps related to body lightening during the evolution of flight [90]. Egg size progressively increased and clutch size decreased during early avian evolution [90].This summary illustrates how the classic anatomical and behavioral features of birds (the bird ‘blueprint’) did not evolve in one or a few spurts of innovation, but more gradually over a long period of evolutionary time and across the dinosaur family tree (Figure 1). However, there apparently were some bursts of evolution in the early history of birds. Once a small flight-capable dinosaur had been assembled, there was a huge spike in rates of anatomical evolution in the earliest birds [2]. Later, the early evolution of short-tailed birds (Pygostylia) in the Cretaceous was associated with high rates of hindlimb evolution and greater than normal speciation [91].

 Birds Dealt with a Crisis at the End of the Cretaceous

The course of avian history was dramatically affected by the mass extinction at the end of the Cretaceous, ∼66 million years ago, which wiped out all non-avian dinosaurs and many other groups [9293]. The extinction was geologically rapid and most likely caused by the impact of a large asteroid or comet, which triggered a global cataclysm of climate and temperature change, acid rain, earthquakes, tsunamis, and wildfires [9495]. It is possible that somewhat longer-term changes in the Earth system, including volcanism and sea-level fluctuations, may have also played a role in the extinction [96]. The emerging picture, however, is that the world changed suddenly at the end of the Cretaceous, killing off many once-dominant groups and giving other organisms an opportunity to radiate in the vacant ecospace.Birds were diverse in the Late Cretaceous, with many of the characteristic lineages of ‘archaic’ birds from the Jehol Biota (species outside of the neornithine crown, such as enantiornithines and basal ornithuromorphs) living alongside what was probably a moderate diversity of early neornithines, as indicated by rare fossils and molecular phylogenetic studies tracing some modern lineages into the Cretaceous [4399798]. None of these ‘archaic’ non-neornithine birds, however, apparently survived past the Cretaceous and into the Paleogene. There has long been debate about whether the extinction of ‘archaic’ birds was gradual or sudden, but recent evidence shows that a diverse avifauna of enantiornithines and basal ornithuromorphs persisted until at least a few hundred thousand years before the end of the Cretaceous in western North America, suggesting that the extinction was sudden and directly linked to the end-Cretaceous impact [99]. This also indicates that birds were strongly affected by the end-Cretaceous extinction, with many major early groups going extinct, countering the stereotype that the mass extinction decimated the non-avian dinosaurs but largely spared birds (see reviews in [9299]). However, because of the scrappy fossil record of the latest Cretaceous birds, which is mostly limited to isolated bones [99], it has been unclear why certain birds went extinct and others survived.Multiple lineages of early neornithines must have endured the extinction, leaving them the only surviving members of the initial Mesozoic radiation of birds. Fossil [100101] and recent genetic [4] evidence supports this view and shows that these birds diversified rapidly in the post-apocalyptic world, probably taking advantage of the ecological release afforded by the extinction of both the ‘archaic’ birds and the very bird-like non-avian dinosaurs. Numerous groups of modern neornithines make their first appearance in the fossil record during the ∼10 million years after the end-Cretaceous extinction [102], and a genome-scale molecular phylogeny indicates that nearly all modern ordinal lineages formed within 15 million years after the extinction [4], suggesting a particularly rapid period of both genetic evolution and the formation of new species (Figure 6). We discuss this recent phylogenomic study further below.

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Figure 6Ordinal-level genome-scale family tree of modern birds. The tree was generated from ∼30 million base pairs of genomic DNA consisting of exons, introns, and ultraconserved elements. Branch colors represent well-supported clades. All bootstrap values are 100% except where noted. Names on branches denote orders (-iformes) and English group terms (in parentheses). To the right are superorder (-imorphae) and higher unranked names. Text color denotes groups of species with broadly shared traits, whether by homology or convergence. The arrow at the bottom indicates the Cretaceous–Paleogene boundary at 66 million years ago, with the Cretaceous period shaded at left. The dashed line represents the approximate end time (50 million years ago) by which nearly all neoavian orders diverged. Horizontal gray bars on each node indicate the 95% credible interval of divergence time in millions of years. Figure used and modified with permission from [4].

Birds after the Cretaceous

The more than 10,000 species of birds living in today’s world are divided into two major groups: the Palaeognathae (which includes flightless forms, such as kiwis, ostriches, emus, and rheas) and the Neognathae, the speciose clade that includes the remainder of bird diversity. The Neognathae, in turn, is composed of the subgroup Galloanserae (the ‘fowls’, including ducks, chickens, and geese) and Neoaves (which includes everything from pigeons and owls to falcons and parrots) [49798103] (Figure 6).The phylogenetic relationships of Neoaves have been the subject of extensive work in recent years. The recent phylogenomic study by Jarvis et al. [4] is the most comprehensive genome-scale analysis of birds to date in terms of amount of DNA sequence (using up to ∼300 million nucleotides) and number of analyses, and attempted to resolve two main issues: firstly, the general branching patterns between the major orders on the bird family tree; and secondly, when these groups diverged, particularly which groups originated before the end-Cretaceous extinction and which arose afterwards. The study was able to resolve, with the highest level of certainty to date, the ordinal relationships of modern birds, and determine that the majority of these groups diverged immediately after the Chicxulub asteroid impact that ushered out the Cretaceous.According to the dated phylogeny of Jarvis et al. [4], the common ancestor of Neoaves lived in the Cretaceous. The earliest divergence of this ancestor gave rise to the major subgroups Columbea (consisting of doves, flamingoes, grebes, and sandgrouse) and Passerea (consisting of all other neoavian species). We predict that this ancestor may have been ecologically similar to modern shorebirds, since the number of divergences after the Columbea and Passerea split, and thereby also after the Neognathae split, to obtain an aquatic or semi-aquatic versus terrestrial species are almost equal (Figure 6) [4]. At least four to six of these basal Neoaves lineages and several members of Palaeognathae and Galloanseres are predicted to have passed through the end-Cretaceous extinction. The subsequent burst of speciation after the extinction consisted of an initial rapid radiation of additional basal Neoaves orders, from grebes to hummingbirds, followed by two subsequent radiations of ‘core waterbirds’ (including penguins, pelicans, and loons) and ‘core landbirds’ (including birds of prey, woodpeckers, parrots, and songbirds). As mentioned above, nearly all of these ordinal divergences occurred within the first 15 million years after the mass extinction, with this pulse of evolution ending around 50 million years ago.In general, the results of the Jarvis et al. [4] study are consistent with earlier studies proposing a major post-Cretaceous radiation of birds [99104] and the hypothesis that shorebird-type species were able to endure the extinction [100101] with traits that may have allowed them to live in diverse environments. However, these new results are at odds with previous molecular studies suggesting a major pre-Cretaceous divergence of Neoaves 20–100 million years earlier [97105106]. The main differences with some previous molecular studies are that the Jarvis et al.[4] study used genomic-scale data and took a conservative approach of using non-ambiguous fossils for dating the tree. In sum, the new phylogenomic study supports a ‘short fuse’ hypothesis for modern bird diversity (e.g. [100]), in which some of the main extant lineages originated during the final few tens of millions of years of the Cretaceous, but the key interval of speciation and ordinal-level diversification was concentrated in the few million years after the end-Cretaceous extinction.The new phylogenetic analysis revealed some surprising relationships among well-known living birds, which help to better understand the evolution of important anatomical and ecological traits. Among the Columbea, the flamingos and grebes (both waterbird orders) were found to be sister clades [107] and their closest relatives were inferred to be a landbird group consisting of pigeons, sandgrouse, and mesites (Figure 6). This suggests that the aquatic or terrestrial adaptations of these groups with the ‘core’ waterbirds and landbirds are convergent. Among the ‘core’ waterbird group, there appears to be a graded acquisition of aquatic traits, beginning with the sunbittern/tropicbird clade and culminating in penguins and pelicans amongst others, which are more obligate water-dwellers.The common ancestor of the ‘core’ landbirds was inferred to be an apex predator, closely related to the extinct giant terror birds (Phorusrhacidae) that included human-sized apex predators in North and South America during much of the Cenozoic (around 62–2 million years ago) [107108]. The species at the deepest branches of ‘core’ landbirds (vultures/eagles/owls and seriemas/falcons) are predatory, but within this group the raptorial trait appears to have been lost twice: once among the Afroaves clade, on the branch leading to Coraciimorphae (mousebirds to bee eaters), and again among the Australaves clade, on the branch leading to Passerimorphae (parrots to songbirds) (Figure 6). The names of Afroaves and Australaves imply their likely geographical origins [109], although more evidence is needed to confirm this. One interpretation of such independent losses of the raptorial trait is that being a predator is a costly lifestyle for modern birds and is being selected against over time. Another interpretation is that this trait was passively lost twice.The new phylogeny also helps to better understand the evolution of one of the most intriguing traits of some living birds: vocal learning, including the ability of some species to imitate human speech. This is a very rare trait, seen in only in songbirds, parrots, and hummingbirds among birds and very few mammals (e.g. dolphins, bats, elephants, and humans) but not non-human primates. As such, avian vocal learners have become highly studied animal models of human speech [110111112]. In contrast to long-standing inferences of three independent gains [103110113], the new analysis supports two independent gains of vocal learning amongst Neoaves: once in the hummingbirds and once in the common ancestor of parrots and songbirds, followed by two subsequent losses in New Zealand wrens and suboscines. However, it does not completely rule out independent evolution in parrots and songbirds (Figure 6) [4]. All three vocal-learning bird lineages and humans were found to have evolved convergent mutations and changes in gene expression in the regions of the brain that control song (bird) and speech (human) [98114]. Overall, these findings reveal the great amount of diversity and convergence that occurred among birds (including some features convergent with mammals) during the post-Cretaceous revolution.

 Conclusions

Modern birds achieved their enormous diversity over a more than 150 million year evolutionary journey, which began with their divergence from theropod dinosaurs, continued with the gradual and piecemeal acquisition of a flight-worthy body plan, and involved two bursts of diversification: first in the Mesozoic when a small, feathered, winged dinosaur was fully assembled, and second when surviving species had the freedom to thrive after the end-Cretaceous extinction. The origin of avian diversity reveals some greater truths about evolution over long timescales, namely that major living groups have a deep history, underwent long and often unpredictable paths of evolution, and were given unexpected opportunities to radiate if they were able to survive mass extinctions that decimated other groups. The flurry of recent work on avian evolution is a prime example of how fossil, morphological, genomic, phylogenetic, and statistical data can be combined to weave an evolutionary narrative, and explain how some of the modern world’s most familiar species became so successful.

Acknowledgments

This work is funded by NSF DEB 1110357, Marie Curie Career Integration Grant EC 630652, an NSF GRF, Columbia University, and the American Museum of Natural History to S.L.B.; and HHMI support to E.D.J. We thank R. Benson, J. Choiniere, A. Dececchi, G. Dyke, H. Larsson, M. Lee, G. Lloyd, P. Makovicky, M. Norell, A. Turner, S. Wang, and X. Xu for discussions with S.L.B.; and E.L. Braun, J. Cracraft, J. Fjeldsa, M.T.P. Gilbert, P. Houde, S. Ho, D. Mindell, S. Mirarab, T. Warnow, and G. Zhang for discussions with E.D.J.

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Article Info

Identification

DOI: https://doi.org/10.1016/j.cub.2015.08.00

Figures

  • Figure 1Summary phylogeny (genealogical tree) of birds.
  • Figure 2Montage of feathered, bird-like non-avian theropod dinosaurs.
  • Figure 3A troodontid dinosaur, one of the closest relatives to birds.
  • Figure 4Montage of bird-like features in non-avian theropod dinosaurs.
  • Figure 5Montage of Mesozoic birds.
  • Figure 6Ordinal-level genome-scale family tree of modern birds.