Rates of dinosaur limb evolution provide evidence for exceptional radiation in Mesozoic birds

Birds are the most diverse living tetrapod group and are a model of large-scale adaptive radiation. Neontological studies suggest a radiation within the avian crown group, long after the origin of flight. However, deep time patterns of bird evolution remain obscure because only limited fossil data have been considered. We analyse cladogenesis and limb evolution on the entire tree of Mesozoic theropods, documenting the dinosaur–bird transition and immediate origins of powered flight. Mesozoic birds inherited constraints on forelimb evolution from non-flying ancestors, and species diversification rates did not accelerate in the earliest flying taxa. However, Early Cretaceous short-tailed birds exhibit both phenotypic release of the hindlimb and increased diversification rates, unparalleled in magnitude at any other time in the first 155 Myr of theropod evolution. Thus, a Cretaceous adaptive radiation of stem-group birds was enabled by restructuring of the terrestrial locomotor module, which represents a key innovation. Our results suggest two phases of radiation in Avialae: with the Cretaceous diversification overwritten by extinctions of stem-group birds at the Cretaceous–Palaeogene boundary, and subsequent diversification of the crown group. Our findings illustrate the importance of fossil data for understanding the macroevolutionary processes generating modern biodiversity.     

The evolutionary origin and diversification of feathers

Progress on the evolutionary origin and diversification of feathers has been hampered by conceptual problems and by the lack of plesiomorphic feather fossils. Recently, both of these limitations have been overcome by the proposal of the developmental theory of the origin of feathers, and the discovery of primitive feather fossils on nonavian theropod dinosaurs. The conceptual problems of previous theories of the origin of feathers are reviewed, and the alternative developmental theory is presented and discussed. The developmental theory proposes that feathers evolved through a series of evolutionary novelties in developmental mechanisms of the follicle and feather germ. The discovery of primitive and derived fossil feathers on a diversity of coelurosaurian theropod dinosaurs documents that feathers evolved and diversified in nonavian theropods before the origin of birds and before the origin of flight. The morphologies of these primitive feathers are congruent with the predictions of the developmental theory. Alternatives to the theropod origin of feathers are critique and rejected. Hypotheses for the initial function of feathers are reviewed. The aerodynamic theory of feather origins is falsified, but many other functions remain developmentally and phylogenetically plausible. Whatever their function, feathers evolved by selection for a follicle that would grow an emergent tubular appendage. Feathers are inherently tubular structures. The homology of feathers and scales is weakly supported. Feathers are composed of a suite of evolutionary novelties that evolved by the duplication, hierarchical organization, interaction, dissociation, and differentiation of morphological modules. The unique capacity for modular subdivision of the tubular feather follicle and germ has fostered the evolution of numerous innovations that characterize feathers. The evolution of feather keratin and the molecular basis of feather development are also discussed.     

L’origine et l’évolution des oiseaux : 35 années de progrès

The origin and evolution of birds: 35 years of progress. Birds are dinosaurs – specifically, small feathered and flighted theropod dinosaurs that probably originated in Laurasia during the Late Jurassic over 140 million years ago. They are most closely related to other small theropods such as dromaeosaurs and troodontids, terrestrial predators that were fleet-footed hunters. The origin of birds is a classic example of two kinds of macroevolution: the phylogenetic origin of the group, and the sequential assembly of adaptations such as flight that are indelibly associated with birds. These adaptations were not assembled all at once. Rather, a great many characteristics associated with birds and flight first appeared in non-avian dinosaurs, where they were used for many purposes other than flight. These included insulation, brooding, and probably display and species recognition. Birds diversified steadily but gradually after their origin, which is identified with the origin of flight (Archaeopteryx); forelimb and other flight-associated features evolved more rapidly than features associated with the posterior skeleton. The first birds grew more slowly than extant birds do, and more like other small Mesozoic dinosaurs; like them, they probably matured sexually well before they completed their active skeletal growth. The origin of flight is not a problem of “trees down” or “ground up,” but rather an examination of the order in which diagnostic flight characters evolved, and what each stage can reveal about the functions and habits of bird outgroups at those evolutionary junctures.     

Wings versus legs in the avian bauplan: Development and evolution of alternative locomotor strategies

Wings have long been regarded as a hallmark of evolutionary innovation, allowing insects, birds, and bats to radiate into aerial environments. For many groups, our intuitive and colloquial perspective is that wings function for aerial activities, and legs for terrestrial, in a relatively independent manner. However, insects and birds often engage their wings and legs cooperatively. In addition, the degree of autonomy between wings and legs may be constrained by tradeoffs, between allocating resources to wings versus legs during development, or between wing versus leg investment and performance (because legs must be carried as baggage by wings during flight and vice versa). Such tradeoffs would profoundly affect the development and evolution of locomotor strategies, and many related aspects of animal ecology. Here, we provide the first evaluation of wing versus leg investment, performance and relative use, in birds—both across species, and during ontogeny in three precocial species with different ecologies. Our results suggest that tradeoffs between wing and leg modules help shape ontogenetic and evolutionary trajectories, but can be offset by recruiting modules cooperatively. These findings offer a new paradigm for exploring locomotor strategies of flying organisms and their extinct precursors, and thereby elucidating some of the most spectacular diversity in animal history.     

FROM FROND TO FAN: ARCHAEOPTERYX AND THE EVOLUTION OF SHORT-TAILED BIRDS

Modern birds have extremely short tail skeletons relative to Archaeopteryx and nonavialian theropod dinosaurs. Long- and short-tailed birds also differ in the conformation of main tail feathers making up the flight surface: frond shaped in Archaeopteryx and fan shaped in extant fliers. Mechanisms of tail fanning were evaluated by electromyography in freely flying pigeons and turkeys and by electrical stimulation of caudal muscles in anesthetized birds. Results from these experiments reveal that the pygostyle, rectrices, rectricial bulbs, and bulbi rectricium musculature form a specialized fanning mechanism. Contrary to previous models, our data support the interpretation that the bulbi rectricium independently controls tail fanning; other muscles are neither capable of nor necessary for significant rectricial abduction. This bulb mechanism permits rapid changes in tail span, thereby allowing the exploitation of a wide range of lift forces. Isolation of the bulbs on the pygostyle effectively decouples tail fanning from fan movement, which is governed by the remaining caudal muscles. The tail of Archaeopteryx, however, differs from this arrangement in several important respects. Archaeopteryx probably had a limited range of lift forces and tight coupling between vertebral and rectricial movement. This would have made the tail of this primitive flier better suited to stabilization than maneuverability. The capacity to significantly alter lift and manipulate the flight surface without distortion may have been two factors favoring tail shortening and pygostyle development during avian evolution.     

A new Chinese specimen indicates that 'protofeathers' in the Early Cretaceous theropod dinosaur Sinosauropteryx are degraded collagen fibres

Alleged primitive feathers or protofeathers in the theropod dinosaur Sinosauropteryx have potentially profound implications concerning feather morphogenesis, evolution offlight, dinosaur physiology and perhaps even the origin of birds, yet their existence has never been adequately documented. We report on a new specimen of Sinosauropteryx which shows that the integumental structures proposed as protofeathers are the remains of structural fibres that provide toughness. The preservation in the proximal tail area reveals an architecture of closely associated bands offibres parallel to the tail's long axis, which originate from the skin. In adjacent more exposed areas, the fibres are short, fragmented and disorganized. Fibres preserved dorsal to the neck and back and in the distal part of the tail are the remains of a stiffening system of a frill, peripheral to the body and extending from the head to the tip of the tail. These findings are confirmed in the holotype Sinosauropteryx and NIGP 127587. The fibres show a striking similarity to the structure and levels of organization of dermal collagen. The proposal that these fibres are protofeathers is dismissed.     

Bipedalism in birds, a determining feature for their adaptive success

The birds are flying animals but they are also basically bipeds. The theropod dinosaurs, precursors of the birds, were already cursorial bipeds. Because the body structure was modelled by aerodynamical constraints during the evolution, all birds, even those that do not fly anymore, share a typical avian body shape. The osteological differences between birds are more adjustments than deep disruptions. Nevertheless, the birds are very diversified in their way of life and habitat. Yet, the hind limbs of the birds are surprisingly efficient in many manners, such as taking off, landing, swimming and walking. The limb structures adaptability to the various tasks require different mechanical fitness or device such as shock absorber during landing, or thrusters during tacking off. Moreover, almost all birds can walk, even if they have another locomotor specialization, as swimming or flying. Depending on the specialization, the gait features of the walk and the kinematics pattern are slightly modified. The functional adaptability of their hind limb structure may be a key to the evolutive success of the birds.     

Air‐filled postcranial bones in theropod dinosaurs: physiological implications and the ‘reptile’–bird transition

Pneumatic (air‐filled) postcranial bones are unique to birds among extant tetrapods. Unambiguous skeletal correlates of postcranial pneumaticity first appeared in the Late Triassic (approximately 210 million years ago), when they evolved independently in several groups of bird‐line archosaurs (ornithodirans). These include the theropod dinosaurs (of which birds are extant representatives), the pterosaurs, and sauropodomorph dinosaurs. Postulated functions of skeletal pneumatisation include weight reduction in large‐bodied or flying taxa, and density reduction resulting in energetic savings during foraging and locomotion. However, the influence of these hypotheses on the early evolution of pneumaticity has not been studied in detail previously. We review recent work on the significance of pneumaticity for understanding the biology of extinct ornithodirans, and present detailed new data on the proportion of the skeleton that was pneumatised in 131 non‐avian theropods and Archaeopteryx. This includes all taxa known from significant postcranial remains. Pneumaticity of the cervical and anterior dorsal vertebrae occurred early in theropod evolution. This ‘common pattern’ was conserved on the line leading to birds, and is likely present in Archaeopteryx. Increases in skeletal pneumaticity occurred independently in as many as 12 lineages, highlighting a remarkably high number of parallel acquisitions of a bird‐like feature among non‐avian theropods. Using a quantitative comparative framework, we show that evolutionary increases in skeletal pneumaticity are significantly concentrated in lineages with large body size, suggesting that mass reduction in response to gravitational constraints at large body sizes influenced the early evolution of pneumaticity. However, the body size threshold for extensive pneumatisation is lower in theropod lineages more closely related to birds (maniraptorans). Thus, relaxation of the relationship between body size and pneumatisation preceded the origin of birds and cannot be explained as an adaptation for flight. We hypothesise that skeletal density modulation in small, non‐volant, maniraptorans resulted in energetic savings as part of a multi‐system response to increased metabolic demands. Acquisition of extensive postcranial pneumaticity in small‐bodied maniraptorans may indicate avian‐like high‐performance endothermy.     

Origin of feathered flight

The origin of flight in birds and theropod dinosaurs is a many-sided and debatable problem. We develop a new approach to the resolution of this problem, combining terrestrial and arboreal hypotheses of the origin of flight. The bipedalism was a key adaptation for the development of flight in both birds and theropods. The bipedalism dismissed the forelimbs from the supporting function and promoted transformation into wings. For the development of true flapping avian flight, a key role was played by the initial universal anisodactylous foot of birds. This foot pattern provided a firm support on both land and trees. Theropod dinosaurs, archaeopteryxes, and some other early feathered creatures had a pamprodactylous foot and, hence, they developed only gliding descent. Early birds descended by flattering parachuting with the use of incipient wings; this gave rise to true flight. Among terrestrial vertebrates, only bats, pterosaurians, and birds developed true flapping flight, although they followed different morphofunctional pathways when solving this task. However, it remains uncertain what initiated the adaptation of the three groups for the air locomotion. Nevertheless, the past decade has provided unexpectedly abundant paleontological data, which facilitate the resolution of this question with reference to birds.     

Body size evolution in Mesozoic birds

The tendency for the mean body size of taxa within a clade to increase through evolution (Cope's Rule) has been demonstrated in a number of terrestrial vertebrate groups. However, because avian body size is strongly constrained by flight, any increase in size during the evolution of this lineage should be limited - there is a maximum size that can be attained by a bird for it to be able to get off the ground. Contrary to previous interpretations of early avian evolution, we demonstrate an overall increase in body size across Jurassic and Cretaceous flying birds: taxon body size increases from the earliest Jurassic through to the end of the Cretaceous, across a time span of 70 Myr. Although evidence is limited that this change is directional, it is certainly nonrandom. Relative size increase occurred presumably as the result of an increase in variance as the avian clade diversified after the origin of flight: a progression towards larger body size is seen clearly within the clades Pygostylia and Ornithothoraces. In contrast, a decrease in body size characterizes the most crownward lineage Ornithuromorpha, the clade that includes all extant taxa, and potentially may explain the survival of these birds across the Cretaceous-Palaeogene boundary. As in all other dinosaurs, counter selection for small size is seen in some clades, whereas body size is increasing overall.     

Theropod forelimb design and evolution

We examined the relationship between forelimb design and function across the 230-million-year history of theropod evolution. Forelimb disparity was assessed by plotting the relative contributions of the three main limb elements on a ternary diagram. Theropods were divided into five functional groups: predatory, reduced, flying, wing-propelled diving, and flighdess. Forelimbs which maintained their primitive function, predation, are similarly proportioned, but non-avian theropods with highly reduced forelimbs have relatively longer humeri. Despite the dramatically different forces imparted by the evolution of flight, forelimb proportions of basal birds are only slighdy different from those of their non-avian relatives. An increase in disparity accompanied the subsequent radiation of birds. Each transition to flightlessness has been accompanied by an increase in relative humeral length, which results from relatively short distal limb elements. We introduce theoretical predictions based on five biomechanical and developmental factors that may have influenced the evolution of theropod limb proportions.     

被视为恐龙的鸟

尽管于 2 0世纪 2 0年代在亚洲地表层首次发现长有羽毛的恐龙和著名的“龙骨突位点” ,关于鸟类起源的争论仍没有休止。来自化石的证据表明 ,鸟类在进化分支上应归于兽脚类的特殊分支。本文主要阐明完好无损的化石揭示的鸟和非鸟类恐龙的亲密关系和鸟类羽毛及鸟类出现以前的羽毛的起源证据 ,分析体型缩小对飞行进化的重要意义及从新的角度论述鸟类如何飞上了天     

Theropod Locomotion

Theropod (carnivorous) dinosaurs spanned a range from chicken-sizedto elephant-sized animals. The primary mode of locomotion inthese dinosaurs was fairly conservative: Theropods were erect,digitigrade, striding bipeds. Even so, during theropod evolutionthere were changes in the hip, tail, and hindlimb that undoubtedlyaffected the way these dinosaurs walked and ran, a trend thatreached its extreme in the evolution of birds. Some derivednon-avian theropods developed hindlimb proportions that suggesta greater degree of cursoriality than in more primitive groups.Despite this, fossilized trackways provide no evidence for changesin stride lengths of early as opposed to later non-avian theropods.However, these dinosaurs did take relatively longer strides—atleast compared with footprint length—than bipedal ornithischiandinosaurs or ground birds. Judging from trackway evidence, non-aviantheropods usually walked, and seldom used faster gaits. Thelargest theropods were probably not as fleet as their smallerrelatives.     

中国中生代鸟类后肢骨骼的长度比例特征及栖息习性的分析

通过对18目59科137例现生不同栖息习性鸟类的后肢3块骨骼(股骨、胫跗骨和跗跖骨)长度比例的观察和特征分析,推断出鸟类的栖息习性与后肢3块骨骼中各骨骼长度所占总长度的比例存在密切的关系。即在所有鸟类的后肢骨骼中,胫跗骨的长度占3块骨骼的比例为最大;地栖鸟类后肢骨骼中股骨的长度要短于跗跖骨;树栖鸟类后肢骨骼中股骨的长度要长于跗跖骨。鸟类后肢3块骨骼的长度比例特征是鸟类长期对栖息等行为适应的结果。在此基础上,对中国中生代14例鸟类的栖息习性进行了分析,利用三元投影的统计方法,并以国内外新生代(古近纪和新近纪)21例鸟类标本作为对比参考,得出辽西中生代不同类型鸟类的栖息行为特征:基干鸟类以树栖为主要习性,其中个别鸟类还具有攀援的习性,而反鸟类则是典型的树栖鸟类,今鸟类兼有树、地栖的习性。研究表明,在现行的鸟类系统发育框架下,树栖适应(及攀援)代表了鸟类演化历史中最原始的生活方式。这一结论也支持鸟类飞行的树栖起源假说。中生代鸟类栖息习性分异的多样性反映了早期鸟类演化过程中自身以及与其他同期生物在生态空间和食物资源的竞争的加剧和对环境的不断适应。     

Coevolution of caudal skeleton and tail feathers in birds

Birds are capable of a wide range of aerial locomotor behaviors in part because of the derived structure and function of the avian tail. The tail apparatus consists of a several mobile (free) caudal vertebrae, a terminal skeletal element (the pygostyle), and an articulated fan of tail feathers that may be spread or folded, as well as muscular and fibroadipose structures that facilitate tail movements. Morphological variation in both the tail fan and the caudal skeleton that supports it are well documented. The structure of the tail feathers and the pygostyle each evolve in response to functional demands of differing locomotor behaviors. Here, I test whether the integument and skeleton coevolve in this important locomotor module. I quantified feather and skeletal morphology in a diverse sample of waterbirds and shorebirds using a combination of linear and geometric morphometrics. Covariation between tail fan shape and skeletal morphology was then tested using phylogenetic comparative methods. Pygostyle shape is found to be a good predictor of tail fan shape (e.g., forked, graduated), supporting the hypothesis that the tail fan and the tail skeleton have coevolved. This statistical relationship is used to reconstruct feather morphology in an exemplar fossil waterbird, Limnofregata azygosternon. Based on pygostyle morphology, this taxon is likely to have exhibited a forked tail fan similar to that of its extant sister clade Fregata, despite differing in inferred ecology and other aspects of skeletal anatomy. These methods may be useful in reconstructing rectricial morphology in other extinct birds and thus assist in characterizing the evolution of flight control surfaces in birds. J. Morphol. 275:1431–1440, 2014. © 2014 Wiley Periodicals, Inc.     

On the origin of avian flight: Compromise and system approaches

Based on evolutionary morphological analysis of the fore and hind limbs of extinct and extant birds, a new compromise hypothesis of the origin of flight in birds and theropod dinosaurs is proposed. The bipedalism and anisodactylous foot suitable for various functions were key adaptations for the development of flight. The bipedalism freed forelimbs from the supporting function and promoted transformation into wings, as animals moved from one tree branch to another and descended from trees. At the initial stage, the strong hind limbs provided the opportunity to climb and leap onto trees, bushes, or eminence, while the anisodactylous foot provided a firm support on both dry land and trees. The support provided by this foot allowed the reduction of the tail, which was initially composed of a long row of vertebrae. Thus, a stage of gliding flight was not necessarily passed by early birds. In the other lineages of feathered creatures, functional changes in forelimbs that resulted in the formation of wings developed in parallel and followed almost the same scenario.     

Assessing arboreal adaptations of bird antecedents: testing the ecological setting of the origin of the avian flight stroke

The origin of avian flight is a classic macroevolutionary transition with research spanning over a century. Two competing models explaining this locomotory transition have been discussed for decades: ground up versus trees down. Although it is impossible to directly test either of these theories, it is possible to test one of the requirements for the trees-down model, that of an arboreal paravian. We test for arboreality in non-avian theropods and early birds with comparisons to extant avian, mammalian, and reptilian scansors and climbers using a comprehensive set of morphological characters. Non-avian theropods, including the small, feathered deinonychosaurs, and Archaeopteryx, consistently and significantly cluster with fully terrestrial extant mammals and ground-based birds, such as ratites. Basal birds, more advanced than Archaeopteryx, cluster with extant perching ground-foraging birds. Evolutionary trends immediately prior to the origin of birds indicate skeletal adaptations opposite that expected for arboreal climbers. Results reject an arboreal capacity for the avian stem lineage, thus lending no support for the trees-down model. Support for a fully terrestrial ecology and origin of the avian flight stroke has broad implications for the origin of powered flight for this clade. A terrestrial origin for the avian flight stroke challenges the need for an intermediate gliding phase, presents the best resolved series of the evolution of vertebrate powered flight, and may differ fundamentally from the origin of bat and pterosaur flight, whose antecedents have been postulated to have been arboreal and gliding.     

Flightless birds are not neuroanatomical analogs of non-avian dinosaurs

Background

In comparative neurobiology, major transitions in behavior are thought to be associated with proportional size changes in brain regions. Bird-line theropod dinosaurs underwent a drastic locomotory shift from terrestrial to volant forms, accompanied by a suite of well-documented postcranial adaptations. To elucidate the potential impact of this locomotor shift on neuroanatomy, we first tested for a correlation between loss of flight in extant birds and whether the brain morphology of these birds resembles that of their flightless, non-avian dinosaurian ancestors. We constructed virtual endocasts of the braincase for 80 individuals of non-avian and avian theropods, including 25 flying and 19 flightless species of crown group birds. The endocasts were analyzed using a three-dimensional (3-D) geometric morphometric approach to assess changes in brain shape along the dinosaur-bird transition and secondary losses of flight in crown-group birds (Aves).

Results

While non-avian dinosaurs and crown-group birds are clearly distinct in endocranial shape, volant and flightless birds overlap considerably in brain morphology. Phylogenetically informed analyses show that locomotory mode does not significantly account for neuroanatomical variation in crown-group birds. Linear discriminant analysis (LDA) also indicates poor predictive power of neuroanatomical shape for inferring locomotory mode. Given current sampling, Archaeopteryx, typically considered the oldest known bird, is inferred to be terrestrial based on its endocranial morphology.

Conclusion

The results demonstrate that loss of flight does not correlate with an appreciable amount of neuroanatomical changes across Aves, but rather is partially constrained due to phylogenetic inertia, evident from sister taxa having similarly shaped endocasts. Although the present study does not explicitly test whether endocranial changes along the dinosaur-bird transition are due to the acquisition of powered flight, the prominent relative expansion of the cerebrum, in areas associated with flight-related cognitive capacity, suggests that the acquisition of flight may have been an important initial driver of brain shape evolution in theropods.

     

The evolution of vertebrate flight

Flight–defined as the ability to produce useful aerodynamic forces by flapping the wings–is one of the most striking adaptations in vertebrates. Its origin has been surrounded by considerable controversy, due in part to terminological inconsistencies, in part to phylogenetic uncertainty over the sister groups and relationships of birds, bats and pterosaurs, and in part to disagreement over the interpretation of the available fossil evidence and over the relative importance of morphological, mechanical and ecological specializations. Study of the correlation between functional morphology and mechanics in contemporary birds and bats, and in particular of the aerodynamics of flapping wings, clarifies the mechanical changes needed in the course of the evolution of flight. This strongly favours a gliding origin of tetrapod flight, and on mechanical and ecological grounds the alternative cursorial and fluttering hypotheses (neither of which is at present well-defined) may be discounted. The argument is particularly strong in bats, but weaker in birds owing to apparent inconsistencies with the fossil evidence. However, study of the fossils of the Jurassic theropod dinosaur Archaeopteryx , the sister-group of the stem-group proto-birds, supports this view. Its morphology indicates adaptation for flapping flight at the moderately high speeds which would be associated with gliding, but not for the slow speeds which would be required for incipient flight in a running cursor, where the wingbeat is aerodynamically and kinematically considerably more complex. Slow flight in birds and bats is a more derived condition, and vertebrate flapping flight apparently evolved through a gliding stage.     

Gravity-defying Behaviors: Identifying Models for Protoaves

Most current phylogenetic hypotheses based upon cladistic methodologyassert that birds are the direct descendants of derived maniraptorantheropod dinosaurs, and that the origin of avian flight necessarilydeveloped within a terrestrial context (i.e., from the "groundup"). Most theoretical aerodynamic and energetic models or chronologicallyappropriate fossil data do not support these hypotheses forthe evolution of powered flight. The more traditional modelfor the origin of flight derives birds from among small arborealearly Mesozoic archosaurs ("thecodonts"). According to thismodel, protoavian ancestors developed flight in the trees viaa series of intermediate stages, such as leaping, parachuting,gliding, and flapping. This model benefits from the assemblageof living and extinct arboreal vertebrates that engage in analogousnon-powered aerial activities using elevation as a source ofgravitational energy. Recent reports of "feathered theropods"notwithstanding, the evolution of birds from any known groupof maniraptoran theropods remains equivocal.