ISSN 00310301, Paleontological Journal, 2010, Vol. 44, No. 12, pp. 15701588. Pleiades Publishing, Ltd., 2010

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INTRODUCTION

The first hypotheses for the origin of flight in birds,which were formulated just after the discovery ofArchaeopteryx in the mid19th century, were diametrically opposite. The major alternatives were thehypothesis of arboreal or trees down (Marsh, 1877) andthe hypothesis of cursorial or ground up developmentof avian flight (Williston, 1879). According to thearboreal hypothesis, birds evolved from thecodonts(Seeley, 1866; Broom, 1913; Heilmann, 1926), whilethe cursorial hypothesis implied that they evolvedfrom running theropod dinosaurs (Huxley, 1868;Gegenbaur, 1878; Osborn, 1900). In the last in his lifetime edition of The Origin of Species, Darwin (1872)noted that Archaeopteryx is a strange bird, with a longtail, as in lizards, each vertebra of which had a pair offeathers, and wings, which had two free claws each; inaddition, he in general adhered to the idea that birdsdescended from dinosaurs.

Birds are unique among terrestrial vertebrates inthe functioning of the locomotor system, with theirforelimbs adapted for flight and hind limbs adapted formovement on land and water. In fact, the two systemsare adapted for movements in essentially differentenvironments. In the evolution of birds, the formationof the system of air locomotion with the use of the

forelimbs and the evolution of their pelvic girdle andhind limbs were tightly connected and correlated.

BRIEF REVIEW OF CONCEPTS OF THE ORIGIN OF AVIAN FLIGHT

The problems of the origin of flight and the originof birds are fundamentally connected. All concepts ofthe origin of flight have been reviewed in detail byShipman (1998) and Paul (2002). At present, twomajor hypotheses of the origin of birds are discussed,i.e., they evolved from either Triassic archosauromorphs through Archaeopteryx or Jurassic theropod dinosaurs, also through Archaeopteryx. According to thearboreal hypothesis, archosauromorph ancestors ofbirds climbed trees, embracing the stem and branchesby the clawed manus, and descended by gliding and,subsequently, turned from gliding to flapping flight(Bock, 1965, 1986; Tarsitano and Hecht, 1980;Feduccia, 1999; Martin, 2004, 2008). According tothe other variant of the arboreal hypothesis, avianflight evolved through gliding of dromaeosaurids,which climbed trees (Chatterjee, 1997b, 1999; Chatterjee and Templin, 2007).

The dinosaurian hypothesis, which is supported bymany researchers and widely popularized by mass

Origin of Feathered FlightE. N. Kurochkina and I. A. Bogdanovichb

aBorissiak Paleontological Institute, Russian Academy of Sciences, Profsoyuznaya ul. 123, Moscow, 117997 Russiaemail: enkur@paleo.ru

bSchmalhausen Institute of Zoology, National Academy of Sciences of Ukraine, ul. Bogdana Khmelnitskogo 15, Kiev, 01601 Ukraine

email: ibogdanovich@rambler.ruReceived March 15, 2010

AbstractThe origin of flight in birds and theropod dinosaurs is a manysided and debatable problem. Wedevelop a new approach to the resolution of this problem, combining terrestrial and arboreal hypotheses ofthe 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 transformationinto 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 incipientwings; this gave rise to true flight. Among terrestrial vertebrates, only bats, pterosaurians, and birds developedtrue 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.

Keywords: Aves, Enantiornithes, Archaeopteryx, Theropoda, Ornithurae, Mesozoic, origin of flight.

DOI: 10.1134/S0031030110120129

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media, has occupied a leading position and oftenseems to provide a conclusive resolution of the problem. Within the framework of this hypothesis, birdsacquired the flight through rapid running of terrestrialtheropods (Fig. 1), then, jumping and gliding, whicheventually resulted in the flight (Ostrom, 1976, 1979,1997; Caple et al., 1983; Mller and Streicher, 1989;Padian and Chiappe, 1998b) (Fig. 1).

A peculiar variant of the terrestrial hypothesis wasdeveloped by Dial (2003b; Dial et al., 2008). As hewatched the rock partridge (Alectoris graeca) climbingan inclined plane, he indicated that, as the angle ofinclination increased, the birds began flapping wingsand, as a result, moved successfully upwards evenwhen the plane was almost vertical. This was particularly typical of nestlings, which were virtually incapable of flying. Similarly, the ancestors of birds couldhave run on slopes by propulsion of movement usingflaps of the forelimbs, which subsequently transformed into wings equipped with the plumage. Whendescending, rudimentary wings and hind limbs ofnestlings actively and synchronously worked, presumably as in remote ancestors of flying birds. Thishypothesis was named the hypothesis of the ontogenetictransitional wing (OTW). This version of thedevelopment of flight corresponds to a certain extentto our reasoning developed below.

Biomechanical studies of the origin of flight basedon the study of Archaeopteryx, either reject the possibility of flight from the ground and at run (Rayner,1985; OFarell et al., 2002; Norberg, 2004) or substantiate the origin of flight just in such a way (Caple et al.,1983; Shipman, 1998; Burgers and Chiappe, 1999).

Garner et al. (1999) rejected both terrestrial (fromrunning) and arboreal hypotheses of the developmentof flight. They proposed an alternative hypothesis of

pouncing proavis. This model implies that the flightdeveloped in predatory ancestors of birds and evolvedfrom pouncing on prey from an eminence or ambush.In attacking proavises, the control of body movementswas improved as the distal part of the forelimbs and thetail acquired simple feathers with bilaterally symmetrical vanes. During subsequent evolution, naturalselection probably supported remiges with an aerodynamic structure producing lifting force. In thishypothesis, a new approach to the analysis of the problem of the origin of flight is applied, the initial adaptation for which is considered to be the ability of bipedalancestors of proavis to get on certain elevations andpouncing on prey from above.

Peters (2002) proposed that climbing adaptationsof the forelimbs are incompatible with flying anddeveloped a variant of the terrestrial hypothesis of theorigin of flight through gliding jumps from an elevatedpoint (such as cliffs or steep slopes), with subsequentflight. In his opinion, the climbing ability gave nothingfor the initiation of flight, while typical features ofavian anatomy, such as the reduction of teeth andclaws of fingers, horny beak, pygostyle, reduced fibula,and secondary loss of flight repeatedly disappearedand appeared in the evolution of birds (Peters, 2000).

All variants of the arboreal hypothesis coincide intwo conclusions, the presence of a gliding stage beforeflapping flight and the recognition of Late JurassicArchaeopteryx from localities of Bavaria as the ancestor of all later birds.

A novel hypothesis for the origin of avian flight wasdeveloped by Thulborn and Hamley (1985) andLoparev (1996) based on the analysis of the pelvicstructure of dinosaurs and birds and ontogeny of livingbirds. According to this hypothesis, early birds developed flight in shallow nearshore biotopes with thickets

Running with help of wings

Horizontal takeoff

Vertical

Aves

Maniraptora

takeoffrunning with help of wings

Fig. 1. Stages of the development of avian flight according to the terrestrial hypothesis (reprinted from Chiappe, 2007, withauthors permission).

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of emergent vegetation. When searching for food inthese biotopes, they spread widely the forelimbs toform a shadow; as a result, the primary plumage transformed into wide flight feathers. When escaping frompredators, they ran on the water surface, using flapping movements of the forelimbs; having reachedthickets, they hid behind them. When moving inthickets, the digits of the forelimbs equipped withclaws were used. This locomotion evolved in glidingand, subsequently, flight above the water, which wasprovided by the development of feathers on the forelimbs; eventually, they acquired the cruising flight. Itshould be noted that a similar hypothesis of theappearance of Protoavis and avian plumage undernearshore conditions was previously proposed byLacasaRuiz (1993). Independently of these authors,Saveliev (2005) developed the hypothesis for the originof birds and avian flight in nearshore habitats, basedon the supposition that the ancestors of birds couldhave consumed rich aquatic food resources, run inshallow water biotopes, and swum underwater usingthe forelimbs; this provided special changes in thecentral nervous system.

We have developed a compromise hypothesis of terrestrialarboreal origin of flight, which is supported bysystemic changes in the locomotor apparatus of thefore and hind limbs and plumage in the evolution ofarchosauromorphs and early feathered reptiles andbased on morphofunctional analysis of the musculoskeletal system of living birds (Kurochkin andBogdanovich, 2008a, 2008b) and on the study of newrecords of the earliest birds and feathered theropoddinosaurs.

HIND LIMBS

Obligatory bipedal locomotion on land, with supporting digits of hind limbs, was acquired even byancestors of theropods and birds (Gauthier, 1986).However, the bipedal patterns of theropods and livingbirds differ essentially (Bogdanovich, 2004; Hutchinson and Allen, 2009). As a bird walks, the femurremains almost immobile, and the step length is determined by the amplitude of movements of the tibia andtarsometatarsus. In theropods, the step length is determined by movements of all three segments of the hindlimb (femur + tibia + metatarsus); however, the steplength is approximately the same as in birds (Jones etal., 2000). These differences in locomotion suggestvery early and independent divergence of birds andtheropods at the level of archosauromorphs (Jones etal., 2000). The combination of cursorial features andlong heavy tail in bipedal theropods and a number ofornithischians has attracted considerable interest(Coombs, 1978). The balancing function of the tailwas understood rather early, for example, by Nopsca(1907) and became generally accepted. Certainly, aheavy tail counterbalanced the anterior part of theinclined trunk of running bipedal animals (Fig. 2).

A probable reason for the development of bipedalism and standing posture was the necessity fordecreasing the load on the femoral curve, as the bodyweight increased in some early archosauromorphs,which became larger (Kubo and Benton, 2007). Transition to facultative bipedalism in lizards is consideredto correlate with prevalence of the support on hindlimbs at an accelerated trot, as short forelegs could notkeep up with hind legs (Sukhanov, 1968). In addition,it should be noted that, in lizards, with their sprawlinglimbs, an increase in efficiency of bipedal running is

Fig. 2. A bipedal archosauromorph, ancestor of ornithuromorph birds; reconstructed by E. Kurochkin, drawn by O. OrekhovaSokolova.

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probably connected with the absence of trunk undulation, which accompanies a quadrupedal locomotion.In contrast to lizards, the limbs of progressive thecodonts and early theropods were not spread apart, butwere positioned in an almost parasagittal plane (Sennikov, 1989; Carrano, 2000), with a constant bipedalism in some of them. Under these conditions, transition to bipedalism does not provide an advantage. Inaddition, it is difficult to imagine a relatively rapid andmaneuverable bipedal running combined with thepresence of a long heavy tail, since the muscularenergy expended for the maintenance of statodynamicbalance increases considerably under these conditions. Among terrestrial vertebrates which have developed bipedal locomotion, a long and heavy tail is onlyretained in lizards, some archosauromorphs (Ornithosuchidae), crocodilomorphs (Sphenosuchidae), manydinosaurs, and early birdlike feathered creatures.Doubt about rapid running of large dinosaurs is basedon the study of theropod tracks and biomechanicalanalysis (Farlow et al., 2000; Hutchinson and Gatesy,2006; Hutchinson and Allen, 2009). These data suggest that they usually walked, while rapider gaits wereinfrequent.

The bipedalism with a parasagittal position of hindlimbs, which dismissed the forelimbs from supportingfunction and promoted the development of jumpinglocomotion (Caple et al., 1983; Nessov and Yarkov,1989), is regarded as the primary key adaptation forspecialized air locomotion of birds (Gatesy and Dial,1996b). In the MiddleLate Triassic, when theropodsand birds probably appeared (Kurochkin, 2006a), allland masses were united in a single continent (Pangea), with humid biotopes and extensive vegetation atthe periphery and open arid, and even superarid,deserted landscapes in the depth of this huge continent(Yasamanov, 1985; Golonka, 2000). Under conditionsof extensive dry and open landscapes (Irisov, 1992) andthin xerophytic forests (Nessov and Yarkov, 1989), asthe authors cited believe, bipedal ancestors of birdsemerged. Certainly, it is highly probable that bipedallocomotion was formed in open landscapes, whichrequired rapid running over long distances, with minimized energy costs. However, available estimates suggest that bipedalism is as good as quadrupedal locomotion with reference to energy economy (SchmidtNielsen, 1984). It is more important that bipedalismdismissed the forelimbs from supporting function,providing them with other functions. Another prerequisite for the use of hind limbs as the major support waspossibly a high position of the head, which wasrequired for better orientation in dense high plants. Allthe above and the reasoning set forth below almostequally concern the ancestors of true birds and the firsttheropod dinosaurs, since, in our opinion, in contrastto the alternative points of view (Chiappe, 2002), basalbirds and theropods from the very beginning of theappearance of bipedal forms and, then, evolved for along time in parallel under the same landscape condi

tions (Kurochkin, 2006b). At the same time, structuralfeatures of the forearm phalanges, humerus, and phalanges of toes strongly suggest that birds (Aves) andwinged dromaeosaurid (Microraptor) independentlydeveloped flight and arboreal mode of life (Senteret al., 2004).

TRANSFORMATION OF THE FORELIMBS INTO WINGS

The fact that the forelimbs were dismissed from thesupporting function was attributed to various functional reasons. They participated to a greater or lesserextent in manipulative function, although some features, such as the reduction of digits IV and V and theirmetacarpals and the other digits tightly adjoining eachother, are in contrast with the manipulative function ofthe manus. Ostrom (1976) hypothesized that the forelimbs of terrestrial ancestors of birds and theropodswere used as a net for catching insects, as they broughttogether their forelimbs covered with featherlikestructures. However, it is hardly possible to captureprey using such a net, since it would be pushed out bythe air flow as the two planes of the forelimbs werebrought together. Note that later Ostrom (1997) abandoned this theory.

Martin (1983) provided cogent arguments againstthis point of view and proposed that the locomotorsystem of ancestors of birds was divided into twoessentially different parts because of adaptation tomovements in trees by leaping and clinging. Referringto the example of arboreal primates, Martin proposedthat this specialization explained the combination inArchaeopteryx of arboreal lifestyle with the development of fused tarsals and elongated tibiotarsus, whichare usually regarded as adaptations for running. Evenif the features indicated are attributable to such a specialization, the adaptation of the forelimbs for climbing trees (embracing stems and branches by themanus) is difficult to propose as a preadaptation to theformation of wings (Peters, 2002), as is usuallyaccepted by the proponents of the arboreal origin ofavian flight. Arboreal vertebrates usually develop agrasping limb, with two foot digits, or only the first,opposed to the others, with forearm digits and theentire manus elongated mostly by their phalanges andstrengthening of the flexors of the shoulder and elbowjoints (Kovtun, 1984). A variant of this limb type isobserved in arboreal Triassic Megalancosaurus(Renesto, 1994). As a pentadactyl plantigrade limbwas initial to archosauromorph ancestors of reptilesand birds and it changed because of similar functionalcauses (in this case, in mammals and birds), it is possible to propose basically parallel development of themorphotype of arboreal limbs in these groups.

We propose different trends in the transformationof the forelimb into avian wing. Protoavis (P. texensis)from the Late Triassic of the United States (Chatterjee, 1991, 1999) provides a notable example of a tran

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sitional condition. Note that flapping directional flightrequires not only long remiges with suitable aerodynamic structure. A downward stroke must be followedby an upward movement of the wing to a position atleast slightly higher than the dorsum. This is only possible in the condition of appropriate orientation of theglenoid of the scapulocoracoid articulation at thepoint of articulation with the humerus. In Archaeopteryx and even Confuciusornis, the glenoid is orientedsuch that it was impossible to raise the wing above thedorsum (Senter, 2006). However, judging from thestructure of the scapulocoracoid articulation, Protoavis was able to raise the wing above the dorsum(original data), although we believe it could not fly(Kurochkin, 1995, 2001). In the manus of Protoavis, thenumber of digits is reduced to three, metacarpals III andIV show initial fusion, and the carpals are partiallyfused with the metacarpals (Fig. 3). Flexion andextension in the carpometacarpal articulation of Protoavis occurred in the plane of the manus. The formation of these structural features of the manus could notbe connected with the presence of an arboreal (climbing) stage of the limb, although Chatterjee (1999) proposed just this stage of climbing tree stems in maniraptorans, with the use of lengthened forelimbs and a firmtail as a support.

The character of articulation between the coracoidand scapula of Protoavis suggests the presence of thesupracoracoid muscle (Chatterjee, 1995, 1999; Kurochkin, 1995, 2001), which is usually regarded as a levator of the forelimb. However, experimental and electromyographic studies have shown that the basic function of the supracoracoid muscle is rapid supination ofthe humerus and the entire wing at the initial phase ofraising the wing (Ostrom, 1997; Ostrom et al., 1999).

ANISODACTYLOUS FOOT AND TAIL

The development of bipedal locomotion wasaccompanied by the change in the body posture,reduction of the forelimbs, and caudal shift of the center of gravity of the body. Apparently, under these conditions, the heavy, rigid tail initially performed boththe primary balancing function and the function of afacultative support. This facilitated considerably themaintenance of equilibrium, as the body acquired avertical position, with the anteriorly directed digits,leaning on the ground, combined with the generallengthening of the hind limb and partial reduction ofdigits.

We believe that further progress directed to ornithuromorph birds was connected with the improvement of the supporting function of the foot by thedevelopment of anisodactyly, with three digits directedanteriorly and the first (internal) digit directed strictlyposteriorly because of articulation with rudimentarymetatarsal I on its plantar (ventral) side (Bogdanovich,2000). The anisodactylous foot type is probably ancestral to the class Aves (Raikow, 1985; Zinoviev, 2008).The data on Protoavis definitely corroborate this evolutionary scenario. The foot of this animal has a welldeveloped first digit, which is positioned opposite toand at the same level as three anterior digits (Fig. 3).Hence, the anisodactyly is already characteristic of thegrade of Protoavis. This is an essential character, sincethe opposition of digit I at the initial stage of bipedallocomotion increased the static stability of animal andrelieved the tail, providing the opportunity to reduceit. The reduction of the tail (an unnecessary counterbalance in cursorial ancestors of birds, which inhabited mountain slopes) was supported by Irisov (1992),although he did not provide detailed substantiated.

Dementiev (1940) indicated that the hind limb ofbirds, with the initially anisodactylous foot, is in general better adapted for walking than for climbing.However, the opposed position of even one welldeveloped digit provides a clasping function of such a limb.

In general, the anisodactyly was probably the initialpattern in the class Aves, which allowed simultaneousbending of anterior digits and hallux (posterior digit),providing adaptation to both embracing branches andwalking and running (Raikow, 1985; Zinoviev, 2008).Living birds with the primary anisodactylous foot caneasily move on both land and branches. Thus, such afoot shows certain functional universalism, whichcould have given rise to all other types of avian foot.

In general, the majority of archosauromorphs, asmany tetrapods, have a pentadactyl foot, with five digits directed anteriorly; in the former, digit V is onlypartially reduced (Ostrom, 1976). Further reductionof foot digits in the course of improvement of terrestrial locomotion, which was connected with transitionfrom plantigrade to digitigrade limb (Severtsov, 1939),is possible to trace using ornithopod and theropoddinosaurs as an example. They developed a tetradactyl

tdIVrad

II

IVIII

I

uln

IIIV

III

(a) (b)

cd2cd3

Fig. 3. Protoavis texensis Chatterjee, 1991 (after Chatterjee, 1995, modified): (a) manus and (b) foot. Designations:(cd2) and (cd3) carpalia distalia 2 and 3, (rad) radiale,(uln) ulnare, (tdIV) tarsale distale IV, and (IIV) digits.

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foot, with the medially projecting first digit. This foottype is termed pamprodactylous (Bock and Miller,1959; Zinoviev, 2008). In theropods, it allowed theadaptation of the foot for rapid terrestrial locomotion.However, it did not provide firm support on a perch(tree branches), as they adapted to the overground layers of plants.

All proponents of the arboreal hypothesis for theorigin of avian flight believe that, as proavis climbedup vertical tree stems, it embraced them by the forelimbs. In our opinion, this assumption is a simple fallacy, since the external orientation of the claw curvature in Archaeopteryx and other early birdlike feathered creatures, such as Jeholornis, along with

theropods, prevented setting on vertical stems. Inaddition, the character of Triassic and Jurassic treesprecluded free upward movements along their stems.The only way up was leaping on lower branches of treesand subsequent upward jumps or movements by grasping one branch after another. Thus, the hypotheticalproavis could leap onto the lower branches of treesfrom the ground, as is observed in the most primitivegalliform curassow (up to 1.5 m without flying) (Bent,1932) and many other representatives of this generalized order, such as turkey, guineafowl, pheasants, andwild hens (original observations), as they get onto treesfor overnight rest. It should be noted that leaps ontotrees or other eminences were repeatedly considered

5 cm

Fig. 4. Skeleton of the ornithuromorph Yixianornis grabaui Zhou et Zhang, 2001 from the Lower Cretaceous of China, with completely opposed first digit of the foot and small pygostyle (indicated by arrows); photograph by E. Kurochkin.

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as a step in the development of flight (Dementiev,1940; Nessov and Yarkov, 1989; Cowen and Lipps,1982; Caple et al., 1983); however, the initial anisodactyly has not been mentioned.

The anisodactylous foot, with simultaneously bending three anterior and one posterior (hallux) digits provided ancestors of birds with firm setting and equilibration on tree branches. Theropods and their feathereddescendants with a pamprodactylous foot lacked a firmseat on branches. By analogy with nestlings of living

birds, it is reasonable to assume that, in ancestors ofbirds (or early birds), jumps on branches and, particularly, downward jumps were accompanied by synchronous flapping and flattering (as termed by Longrich,2006) movements of the forelimbs, which wereintended to maintain equilibrium. When descending,feathered theropods and Archaeopteryx used flatter gliding, which resulted in the formation of true flight, asLong et al. (2003) concluded. Possibly, the distal segments of the forelimbs of ancestors of birds were cov

I

II

III

IV

I

IIIII

Fig. 5. Archaeopteryx grandis Elzanowski, 2001, Solnhofen (sixth) specimen, skeleton; arrows indicate claws of wing digits curvedexternally and foot digit I oriented medially; Roman figures designate digits of the fore and hind limbs; photograph by E.N. Kurochkin.

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ered with lengthened contour feathers, which were usedin display behavior, similar to that of Caudipteryx orProtarchaeopteryx from the Early Cretaceous of China(Ji et al., 1998, 2001).

Consequently, the anisodactylous foot had a significant effect on the trend of subsequent evolution ofbipedal ancestors of true birds and birds themselves.This exaptation provided firm movements on land andstable position on tree branches without the use of thelong tail formed of many vertebrae as a counterbalance. The following paleontological data verify thishypothesis. In the Early Cretaceous Chinese ornithurines Yixianornis, Archaeorhynchus, Hongshanornis,Jianchangornis, and Gansus, the caudal region isformed of 57 short free vertebrae and a shortmediolaterally flattened pygostyle, while digit I of thefoot is distinctly opposed to the others (Fig. 4), so thatthe first metatarsal comes onto the plantar side of thetarsometatarsus (Gansus, Liaoningornis, Yanornis,Yixianornis) (Hou and Liu, 1984; Hou, 1997; Zhouand Zhang, 2001, 2005, 2006; Clarke et al., 2006; Youet al., 2006). Note that fossil tracks from Argentinadetermined as Late Triassic birdlike footprints (Melhor et al., 2002) were produced by a completely anisodactylous foot. Yixianornis is so far the only Early Cretaceous ornithuromorph that retains a relatively shortfanshaped tail, which was positioned on a flattenedpegshaped pygostyle (Clarke et al., 2006).

Theropods, archaeopteryxes, and enantiornithinesfollowed different pathways in the evolution of thehind limb and tail. In particular, in dromaeosaurids,digit I is not opposed to other digits, it is only slightlydisplaced medially and lifted proximally (Norell andMakovicky, 1997). In gliding Microraptor gui, digit I ofthe foot is not opposed (Xu et al., 2003; original data).In the new Late Jurassic fourwinged troodontidAnchiornis huxleyi, the same condition of digit I is alsoevident (Xu et al., 2009). There is no doubt that dromaeosaurids and troodontids from the Upper Jurassicand Lower Cretaceous of China were fourwingedand displayed certain anatomical features, since several hundred fossil specimens have been recorded(Alexander et al., 2010).

It is generally accepted that, in Archaeopteryx, digitI was opposed to other digits of the foot (Feduccia,1999; Feduccia et al., 2007). In fact, Archaeopteryxshows incomplete opposition of digit I (Fig. 5). Thefirst metatarsal is located on the medial surface of thesecond metatarsal; therefore, digit I is directed medially; it could be abducted only slightly posteriorly(Mayr et al., 2005; original data). Therefore, featheredtheropods, Archaeopteryx, and early birdlike taxa,such as Zhongornis, Jinfengopteryx, and Jeholornis,could not get rid of their long tail, since it was a counterbalance, as they leant on three anterior digits of thefoot, which provided insufficiently stable support onboth land and trees. The long digits with large curvedclaws were probably preserved in the forelimbs of these

animals because of the same reason and were used forclutching at branches, as they moved in trees (Fig. 6).

The short proximal and lengthened distal phalanges of wing digits (Zhou and Farlow, 2001) and external curvature of claws of Confuciusornis (as in Archaeopteryx) are poorly adapted for climbing verticalstems, embraced by the forelimbs (Fig. 6). In addition,the short and proximally shifted first digit of Confuciusornis prevented active movements in the tree crown(Zinoviev, 2009). It remained uncertain for a long timehow Archaeopteryx used the externally curved claws(which are distinctly seen in almost all specimens) forclimbing vertical stems of Jurassic trees. Surprisingly,this point escaped attention of researchers. Moreover,there were wide discussions concerning the extent ofclaw curvature compared to living treeclimbing birdsand mammals, as a tool for sticking in tree stems. Thecurved claws of wing digits are also externally orientedin the Early Cretaceous dromaeosaurid Microraptor(Fig. 7) and in Zhongornis and Jinfengopteryx of uncertain relationships (Ji and Ji, 2007; Gao et al., 2008).However, this external orientation of claws looks normal, taking into account that they were adapted forclutching at tree branches, using the widely laterallyspread forelimbs. This assumption is supported by theexternal orientation of the claw curvature in the allularand first digits of the wing of hoatzin nestlings (Opisthocomus), which move in trees clutching at treebranches using the widely spaced wings (Heilmann,1926). It is noteworthy that, even in Early Cretaceousornithurines (Ambiortus, Gansus, Yixianornis, Archaeorhynchus, and Hongshanornis), the ungual phalangesof wing digits were small and only slightly curved(Kurochkin, 1982, 1999; Zhou and Zhang, 2005,2006a; You et al., 2006) (Fig. 8). They had no need oflarge curved claws of wings, since the anisodactylousfoot provided firm seat of birds on branches. An exception is provided by large Early Cretaceous Jianchangornis microdonta, in which the relatively large ungualphalanges of allular and first digits are curved insideand, in addition, the allular digit projects noticeablydistally beyond the edge of the carpometacarpus(Zhou et al., 2009).

In enantiornithines from the Lower Cretaceous ofSpain and China, the caudal region of the vertebral column and digit I (hallux) display different conditions.Iberomesornis from the Lower Cretaceous of Spain haseight relatively wide and long free caudal vertebrae; verylarge and long pygostyle, which is expanded and flattened ventrally, formed of 1015 fused vertebrae; andhallux, which is directed medially and can be turnedposteriorly (Sanz and Bonaparte, 1992; Sereno,2000). In Early Cretaceous Concornis from Spain, thereduced first metatarsal lies on the medial side of thesecond metatarsal; the shape of the proximal articularsurface of digit I suggests that it was limited in posterior rotation (Sanz and Buscalioni, 1992; originaldata); in the caudal region, only two anterior free vertebrae are preserved; therefore, it is impossible to

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reconstruct with certainty the general structure of thecaudal region. In the small enantiornithine Dalingheornis (with a 2cmlong skull) from the Yixian Formation (Liaoning, China), the tail is represented by a2cmlong row of 20 free caudal vertebrae; digits I andII are turned medially (Zhang et al., 2006). Anothersmall Chinese enantiornithine Cathayornis has eightrelatively large free caudal vertebrae and an elongatedpygostyle (15 mm long), which is flattened dorsoventrally and has a wide bifurcating base (Zhou, 1995).Unfortunately, the foot structure of this animalremains uncertain, since the phalanges of its digits aredisarticulated and scattered. Cuspirostrisornis, a relatively small Early Cretaceous enantiornithine fromChina, distinctly shows a large pygostyle and mediallypositioned first digits of feet. In another enantiorni

thine, Rapaxavis, the pygostyle is even larger and morewidened, and the first digit is oriented distinctly medially (Morschhauser et al., 2009). In other large andsmall enantiornithines from the Lower Cretaceous ofChina, the feet of which have been examined (Protopteryx, Sinornis, Eoenantiornis, and Vescornis), thefirst metatarsal lies on the medial side of the secondmetatarsal (Zhang and Zhou, 2000; Sereno, 2002;Zhang et al., 2004; Zhou et al., 2005); this suggeststhat the hallux was incompletely posteriorly turned.Thus, in the majority of known enantiornithines, thenumber of free caudal vertebrae is reduced to 58;however, they are large, widened, and elongated, and along, massive, dorsoventrally flattened pygostyle isattached to them. This suggests that the tail of enantiornithines was relatively heavy and elongated rather

Fig. 6. Carpal region of skeletons of Jeholornis prima Zhou et Zhang, 2002 (upper) and Confuciusornis sanctus Hou et al., 1995(lower) from the Lower Cretaceous of China; arrows indicate claws of externally curved wing digits (after Hou, 1997); photographby E. Kurochkin.

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than fanshaped, with caudal feathers arranged insequential rows, at least, within the distal part of thetail (Fig. 9); therefore, the tail structure was similar tothat of Archaeopteryx. In the foot of Early Cretaceousenantiornithines, digit I was incompletely opposed toother digits. In living ornithuromorph birds, the firstmetatarsal usually lies on the medioplantar margin ofthe second metatarsal. In Late Cretaceous enantiornithines, the tail was probably retained elongated andheavy, as was reconstructed by Martin (1995). Nanantius from the Upper Cretaceous of Mongolia probablyhad a rudimentary pygostyle in the shape of a shortrodlike structure (Kurochkin, 1996).

Evolutionary changes from the elongated leafliketo short fanshaped tail were influenced by aerodynamic requirements. Gatesy and Dial (1996) haveshown that the lifting force produced by the fanshaped tail of extant birds is several times as great asthat of the elongated leaflike tail of Archaeopteryx, allother things (weight, surface area) being equal. Inaddition, they developed the concept of three locomotor modules, i.e., the forelimbs, hind limbs, and tail,which distinguish birds from the unimodular design oftheir bipedal terrestrial ancestors (Gatesy and Dial,1996b; Gatesy, 2002). In their opinion, each avianmodule evolved independently. In contrast, we believethat evolutionary changes in the three modules weretightly correlated.

DISCUSSION

Thus, the model proposed for morphoecologicalevolution of the ancestors of birds implies the initialstage of terrestrial specialization, bipedalism, development of the upward leap (from ground to tree branchesor bushes), subsequent arboreal adaptation throughthe movement along branches by leaping and descentby flattering parachuting (Fig. 10). This evolutionaryscenario assumes the initial specialization of hindlimbs for bipedal locomotion based on the anisodactylous foot, which differs essentially from the foot oftheropods. A probable role of leaping, with the balancing forelimbs for the origin of flight was repeatedlyproposed by supporters of both arboreal and terrestrialhypotheses (Nopsca, 1907; Caple et al., 1983; Nessovand Yarkov, 1989; Padian and Chiappe, 1998a).

The adaptation for the arboreal lifestyle of archosauromorph ancestors of birds is in need of explanation. We believe that this was intended not only forexpansion over new trophic niches but also for avoidance of terrestrial predators, in particular, during thenight and rest, and for the development of nestingadaptations in trees or bushes, which undoubtedlyprovided better defense than on the ground (Bock,1986; Nessov and Yarkov, 1989; Dial, 2003a). Newtrophic niches were developed later, after the formation of true flight. Initially, these animals were apparently small; when leaping down from trees, they lowered relatively slowly; this facilitated the development

of flight. Bock (1986) even proposed that the development of arboreal adaptations in the ancestor of birdsled to a decrease in size.

Turning to the arboreal origin of flight accordingto the scheme from abovedownwards, from a climbing ancestor with the forelimbs embracing branchesand stems, it should be noted that this was connectedwith certain rearrangements in the forelimbs, in particular, with the formation of a prehensile manus,which is incompatible with subsequent changes in theplane of its bending and in the wing. The arborealhypothesis in pure form also implies the stage of gliding (Bock, 1986; Feduccia, 1999). However, the onlygeneral pattern of the evolution of movements in theair through the improvement of gliding is expansion of

Fig. 7. Skeleton of fourwinged Microraptor gui Xuet. al., 2003 from the Lower Cretaceous of China; arrowsindicate remiges of advanced aerodynamic structure onthe fore and hind limbs and wing digits, with externallycurved claws; photograph by E. Kurochkin.

ZinziHighlight

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the flying membrane. Vivid examples of perfect glidersare the flying lemur (Cynocephalus), flying squirrels(Pteromys), marsupial cuscuses, and flying phalangerscan be supplemented by extant and extinct lizards,Sharovipteryx, and Late Permian weigeltisaurids, theearliest known gliders (Bulanov and Sennikov, 2006).However, none of tetrapod groups are known to evolvefrom gliding to flapping flight, that is, groups withgliding primitive forms and advanced forms showingflapping flight (Long et al., 2003). Gliding is providedby an essentially different pattern of morphologicaladaptations compared to active flight (Padian, 1983).In gliders, the plane of the membrane (wing) probablybegins the formation from the body, from its proximalregions in the distal direction. This design is initiallystronger and more efficient aerodynamically, since itdoes not produce a slit between the flying surface andbody nor a narrowing between the left and right membranes. On the contrary, as the avian wing was developed, the flapping plane most likely arose at the distalend of the forelimb, beginning from digits; this is supported by all presently known examples of the development of primary wings from the fore and hind limbsin Mesozoic theropods and early birds: fourwingedMicroraptor and Anchiornis and some enantiornithines(Xu et al., 2003; Zhang and Zhou, 2004; Hu et al.,2009). In flapping wings, the distal regions are best

adapted for interaction with the air, making the majorcontribution to the lifting force and moving more rapidly than the proximal regions of the wing. Thus, gliding is incompatible with subsequent development offlapping flight (Caple et al., 1983).

The formation of featherlike structures predetermined a different trend in the development of the locomotor apparatus in the ancestors of birds. The wing, theapex of which is formed of separate, mobile feathers(wing with a split apex) provided a much greater angleof attack without a burble; this produced sufficient lifting force to support the body in the air, even when thewing moved at a low speed (Yakobi, 1966; Alexander,1970). What was the reason for the formation of primaryfeathers with symmetric vanes on the distal segments ofthe forelimbs and tail of theropod dinosaurs and ancestors of birds? We subscribe to the views of Cowen andLipps (1982) that such a plumage could have developedby sexual selection as an element used for display behavior. This new formation was very useful to maintainequilibrium, as animals moved on tree branches orbushes. The flight, which was initiated by descend fromtrees and evolved from flattering movements (Longrich,2006) of the primarily feathered forelimbs, probablycontributed to the reduction of muscle mass of hindlimbs to a lesser extent than in the case of a continuousflying membrane of bats; this favored further parallel

Fig. 8. Distal wing part of the ornithuromorph Ambiortus dementjevi Kurochkin, 1982 from the Lower Cretaceous of Mongolia;arrows indicate rudimentary and slightly curved claw of wing digit I and imprints of remiges; photograph by E. Kurochkin.

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improvement of both systems. Note that, in Early Cretaceous ornithuromorph birds, flying plumage on thehind limbs has not been recorded. However, in glidingtroodontids, dromaeosaurs, enantiornithines, andArchaeopteryx, the hind limbs had feathers, whichincreased the total lateral surface, although they werecharacterized by poor air locomotion (Feduccia, 1999;Xu et al., 2003, 2009; Christiansen and Bonde, 2004;Zhang and Zhou, 2004; Xu and Zhang, 2005; Longrich, 2006; Hu et al., 2009).

Embryological studies of living birds have shown thatthe foot and manus stop development as a pentadactyllimb (because of fusion of skeletal elements) at approximately the same stage; this also suggests relatively synchronous specialization of the fore and hind limbs in theevolution of birds (Kovtun et al., 2003). It is usuallyaccepted that birds and saurischian dinosaurs were similar in the initial evolutionary stage next to archosauromorph ancestors (Romer, 1923; Walker, 1977). The twogroups probably evolved from different ornithosuchidgroups with the early acquired bipedalism.

Subsequent evolutionary events, which determineddistinctive characters of the ornithuromorph phyleticlineage, probably involved the following features. Thereduced tail and strengthened thoracic musculaturecaused a cranial displacement of the center of gravity.To restore the optimum position (in birds, the centerof gravity is directly above the knee joint and the supporting foot), the position of the femur was changed.In contrast to thecodonts and dinosaurs, the femur ofbirds is positioned closer to the horizontal; this wasindicated earlier without special reasoning (Walker,1977; Chiappe, 1995), and Gatesy (1990) provided afunctional explanation that involved the need to displace the foot under the center of gravity, which inbirds is shifted more cranially than in bipedal theropods. At the same time, an almost horizontal positionof the femora of birds requires a greater abduction ofthese bones (a more lateral position to pass the bodyby) and strengthening the muscles that restrict protractionsupination of the femur to prevent sagging ofthe body between the knee joints. The supination (outward rotation) of the femur combined with the pro

Fig. 9. Reconstructed appearance of the enantiornithine Nanantius valifanovi Kurochkin, 1996 from the Upper Cretaceous ofMongolia; note lengthened tail and dorsoplantarly flattened tarsometatarsus, with medially directed first digits of the foot; reconstructed by E. Kurochkin, drawn by O. OrekhovaSokolova.

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VIII

VI

V

VII

IV

III

III

Fig. 10. Sequence of hypothetical stages of the development of flight in true birds: (I) bipedal terrestrial archosauromorph;(II) development of anisodactyly in archosauromorph ancestor of true birds; (III) leaping on lower branches of trees and bushes;(IV) firm seat on perches at the stage of completely formed anisodactylous foot and initial reduction of long tail; (V and VI) development of feathers with symmetrical vanes on the distal segments of the forelimbs and tail for display behavior; these featherscould decrease the speed of descent by parachuting; (VII) formation of asymmetrical aerodynamic feathers on wings and reduction of long tail; and (VIII) transition to true flapping flight; reconstructed by E. Kurochkin, drawn by O. OrekhovaSokolova.

traction (anterior displacement) provide a mechanismthat places the supporting foot in the projection of thecenter of gravity to maintain equilibrium at the phaseof support on one hind limb (Stolpe, 1932; Hutchin

son and Gatesy, 2000). The protraction of the femur iscontrolled by massive posterior femoral muscles(according to the major function, retractors of thefemur), which are similar in birds and other bipedal

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archosaurs (Bogdanovich, 2005). Regarding therestriction of supination, birds resolved this taskthrough the dorsal displacement of the iliotrochanteric muscles along the lateral surface of the femoralhead and general strengthening of these muscles (themajority of birds have three). These muscles arehomologous to the iliofemoral and puboischiofemoralmuscles of thecodonts and dinosaurs (Hutchinson,2001). In birds, the strengthening and displacement ofthese muscles (cranial or dorsocranial, respectively)resulted in an increase in size of the preacetabularregion of the ilium, which is characteristic of Protoavis. Some researchers believe that the enlargementof this part of the ilium is connected with the supinatorand protractor functions of the iliotrochanteric muscles, as the femur performed wobbling movementsduring running (Hutchinson, 2001). However, thetopography and inner structure of these muscles in living birds (complex pinnate structure, with relativelyshort fibers and a large angle of pinnation) and theelectromyographic study strongly suggest that theyfunction as pronators or extensors of the femur, whenturning movements are performed, and as stabilizersof the femur in the static state (Gatesy, 1999); however,the major function is restriction of supination (Sychet al., 1985).

CONCLUSIONS

The above review of hypotheses for the origin offlight and our morphofunctional analysis of terrestrialand air locomotion and locomotor apparatus of birdsallows the development of a compromise hypothesisfor the origin of flight that combines elements of various variants of terrestrial and arboreal hypotheses withnew data and conclusions. This hypothesis is based onthe system approach to the appraisal of correlated evolutionary changes in the locomotor system and integument of the ancestors of feathered creatures. Theonly element adopted from the terrestrial hypothesis isbipedalism, the key adaptation which dismissed theforelimbs from the supporting function. In contrast tothe arboreal hypothesis in pure form, we propose thattransition of the ancestors of birds onto trees developed through leaping on the lower branches with theuse of support on the hind limbs rather than throughclimbing on the tree stem, with embracing by the forelimbs. In the ancestors of birds, this was possible dueto the early development of the anisodactylous footand true intertarsal joint, which provided a stable support on both the land surface and perches, with tightembracing by completely opposed digit I. Thus, theforelimbs remained freely flapping for the maintenance of equilibrium and development of a flappingwing, as animals descended from trees. The anisodactylous foot, which provided a firm support on fourwidely spaced digits, was the basis for the reduction oflong tail, formed of a series of vertebrae, which wasused by the ancestors of birds for the maintenance of

equilibrium on land and for arboreal locomotion. Thisevolutionary scenario obviates the necessity of a gliding stage in the development of flapping flight, sincethe wing and aerodynamic evolution of its plumage areformed through equilibration by the forelimbs at leaping onto branches and through flattering movementsduring descent.

The elaboration of this evolutionary scenario of theorigin of flight inevitably leads to the recognition of successive stages of the appearance of certain aberrations,selection of which resulted in each new stage of the evolutionarily adapted equilibrium (Shishkin, 2005). However, the mechanism of this process was not restricted toisolated events; on the contrary, it involved correlatedsystemic changes (Shishkin, 2006), including new formations in the fore and hind limbs, caudal module,breathing, integument, behavior, and, eventually, in theentire organization of the living system, as it adapted toessentially new conditions.

The ecological aspect of our hypothesis raises thequestion of under which conditions and why animalswere made to leap onto trees or bushes, equilibrateusing the primary wings, and descend by the flatteringflapping rather than gliding. In the Triassic and Jurassic, the shrub and tree vegetation was dominated byvarious gymnosperms, i.e., Coniferae, Bennettitaceae, Pteridospermae, Cycadaceous, Gnetaceae, andGinkgoaceae. Many of these plants are characterizedby dense branching or feathering just from the groundlevel and dense arrangement of branch whorls alongthe stem (Takhtajan, 1956). It is rather difficult toclimb such trees and bushes along the stem, whileleaping or flying onto projecting branches or feathersand upward jumps in these plants, clutching atbranches by wing digits with claws, are much easier(Fig. 10). In addition, it was probably easy to buildprimitive nests on these dense trees, so that the nestswere well hidden beyond the reach of terrestrial predators. Moreover, the Coniferae, Ginkgoaceae, andGnetaceae provided animals with rich and diverse fruitand seed food. As an animal descends from the tree, itseems less efficient to spring downwards using thesame branches, while gliding with the help of rudimentary wings is difficult or even impossible. Themost suitable way in such a situation is almost verticalparachuting, controlled by flattering flapping movements of the loaded forelimbs (primary wings). Nestlings of extant birds, with the precocial or semiprecocial developmental types (some anseriforms andcharadriiforms), descend from nests located on treesor rocks using the same flatteringparachuting flight.In early birds, such wings could have performed activeposterodorsal flaps, initiating progressive developmentof the supracoracoid muscle. This is the ecologicalbasis and an additional functional aspect of thehypothesis proposed for the origin of flight in trueornithurine birds.

In theropod dinosaurs, digit I is not opposed to theother digits of the foot; the same is true of their direct

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descendants, archaeopteryxes and microraptors. Thisprevented the reduction of the long tail formed of vertebrae, since this foot did not provide a firm support onbranches nor when landing (Fig. 5). Therefore, theycould not develop a true flight, only some became goodgliders, with the supporting area enlarged by the feathersurfaces of the tail and hind limbs. In enantiornithines(probable descendants of archaeopterygids), digit I ofthe foot was incompletely opposed, and the tailremained lengthened due to large extended free caudalvertebrae and long massive pygostyle, the feathers ofwhich were arranged successively rather than formed afanshaped structure.

ACKNOWLEDGMENTS

We are sincerely grateful to L.P. Tatarinov,A.N. Kuznetsov (Zoological Museum of MoscowState University), N.V. Zelenkov, and A.K. Agadjanian (Borissiak Paleontological Institute, RussianAcademy of Sciences), and V.D. Gulyaev (Institute ofAnimal Systematics and Ecology, Siberian Branch,Russian Academy of Sciences) for useful advice andremarks on the manuscript of this paper. We are thankful to the artist O. OrekhovaSokolova for producingfigures illustrating our concept and to Zhonghe Zhoufor the opportunity to study and take photographs ofLower Cretaceous specimens housed in the Instituteof Vertebrate Palaeontology and Palaeoanthropolgy ofChinese Academy of Sciences.

The study of E.N. Kurochkin was supported by theRussian Foundation for Basic Research, projectno. 070400306.

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