tauk 119 140.1 17 - Yale University

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The AukA QuarterlyJournal of Ornithology

Vol. 119 No. 1 January 2002

The Auk 119(1):1–17, 2002

PERSPECTIVES IN ORNITHOLOGY

WHY ORNITHOLOGISTS SHOULD CARE ABOUT THE THEROPODORIGIN OF BIRDS

RICHARD O. PRUM1

Department of Ecology and Evolutionary Biology, and Natural History Museum, University of Kansas,Lawrence, Kansas 66045, USA

OVER THE LAST 25 years, few topics in sys-tematics and paleontology have been as divi-sively debated as the origin of birds (Padianand Chiappe 1998; Feduccia 1999a, b; Dalton2000). For most of the middle of the twentiethcentury, G. Heilmann’s (1926) monumentalanalysis of the topic reigned unchallenged.Heilmann established definitively that birdsare members of the Archosauria (the large rep-tilian clade that also includes crocodiles, ptero-saurs, and dinosaurs). But Heilmann was un-able to accept the voluminous evidence hegathered that placed birds within the carnivo-rous theropod dinosaurs because theropodsapparently lacked a furcula, and Heilmann be-lieved that lost features cannot re-evolve (Dol-lo’s law). Instead, Heilmann (1926) concludedthat birds had evolved from ‘‘thecodonts’’—apolyphyletic garbage bag assemblage of earlyarchosaurs. It is a tribute to the careful detail ofHeilmann’s treatise that his hypothesis was soinfluential given his own ambivalence about hisconclusions. Heilmann described his thecodonthypothesis as ‘‘wholly without shortcomings’’(i.e. character conflict) while essentially admit-ting that there was no evidence other than avi-an membership in the archosaurs to support it.Heilmann’s hypothesis became unquestionedorthodoxy and was the basis of many scenarios

1 E-mail: [email protected]

for the evolution of birds and feathers (e.g. Bock1965).

In 1974, John Ostrom (1974) challenged thestatus quo by revitalizing the old hypothesisthat birds were related to dinosaurs (Huxley1868, 1870; Williston 1879) or, more specifically,to a group of the meat-eating theropod dino-saurs, represented by Deinonychus which hehad recently described. Jacques Gauthier (1986)subsequently confirmed that birds were a lin-eage of theropod dinosaurs most closely relat-ed to dromaeosaurs (the lineage now common-ly known as ‘‘raptors’’), and that result hasbeen generally confirmed by subsequent work-ers (Gauthier et al. 1988; Holtz 1994; Sereno1997, 1999; Forster et al. 1998; Makovicky andSues 1998; Zhou et al. 2000). The last 25 yearshave revealed many paleontological discover-ies that have greatly expanded our knowledgeand understanding of the diversity of theropoddinosaurs and Early Cretaceous birds. The re-sult has been a steady increase in support fortheropod origin of birds, despite arguments tothe contrary (e.g. Martin 1983a, b, 1985; Fed-uccia 1985, 1999a, b; Ruben et al. 1997; Feducciaand Martin 1998; Dodson 2000; Martin andCzerkas 2000; Jones et al. 2001). However, withfew exceptions (e.g. Whetstone and Martin1981; Martin 1983a, b), critics have not pro-posed any explicit alternative hypothesis moredetailed than Heilmann’s (1926) original vaguethecodont notion.

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The debate on bird origins has frequentlybeen portrayed by critics of the theropod hy-pothesis as a battle between ‘‘paleontologists’’and ‘‘ornithologists’’ (Feduccia 1999b). How-ever, this analogy has been allowed to persistfor decades because of the lack of ornithologi-cal participation in the debate rather than anygeneral concordance of ornithological opinion.The lack of ornithological participation in thisdebate can be well documented: a computersearch of the recent volumes of North Ameri-can ornithological journals yields no researchpapers including the word dinosaur in the text.As far as I know, Zhou’s (1995) paper on Mon-onychus is the only article to appear in a majorornithological journal that deals even tangen-tially with the issue of avian origins since Mar-tin et al. (1980).

Why is there so little ornithological interestand involvement in the question of bird ori-gins? With covers and articles in Science, Nature,Scientific American, Audubon, and National Geo-graphic, it cannot be because ornithologists arenot aware of it. There are two primary reasons.First, most ornithologists have not become fa-miliar enough with the primary literature de-scribing the various characters to consider theevidence for themselves. Further, few ornithol-ogists have formal paleontological training,and some may have relied on the criticism of afew to form the opinion that the evidence sup-porting the theropod hypothesis is flawed. Thesecond reason is that many ornithologists aresatisfied that the issue is irrelevant to their re-search and teaching. Like many natural histo-rians over many centuries, ornithologists aregenerally convinced of the peculiar uniquenessof birds, because we gain our professional iden-tities as ‘‘ornithologists’’ from it. Focusing onthe apparent uniqueness of birds may reinforceour professional identities or self esteem, but itmay not help us do the best possible ornitho-logical research and teaching.

Why should ornithologists care about thetheropod origin of birds? Because the theropodorigin of birds is relevant to almost all aspectsof avian biology and should influence the waywe think about, study, and teach avian anato-my, behavior, physiology, ecology, and evolu-tion. Here, I present my perspective on the ev-idence supporting the theropod origin of birds,the criticisms of the hypothesis, and the rele-vance of the theropod origin to ornithology in

hopes of generating a renewed interested andattention to this question within the ornithol-ogy community.

EVIDENCE FOR THE THEROPOD ORIGIN

OF BIRDS

Evidence in support of the theropod origin ofbirds comes from all available sources of pale-ontological evidence—largely osteology, infer-ences about physiology and behavior, andmore recently a variety of fossilized feathers.Since Gauthier (1986) produced the first phy-logenetic analysis of the origin of birds, sup-port of the theropod origin of birds has beenrepeatedly upheld in phylogenetic analyses(e.g. Benton and Clark 1988; Gauthier et al.1988; Holtz 1994; Sereno 1997, 1999; Forster etal. 1998; Makovicky and Sues 1998). All anal-yses have supported the same position forbirds, within a group of higher coelurosauriantheropods which are called maniraptorans—agroup that includes dromaeosaurs, or raptors(e.g. Deinonychus, Velociraptor) and troodontids(e.g. Troodon) (Fig. 1). There have been and con-tinue to be vigorous debates about the relativepositions of various theropod groups that pro-vide opportunities for disagreement among re-searchers (e.g. tyrannosaurs and troodontids;Holtz 1994; Sereno 1997, 1999; Makovicky andSues 1998), but all analyses have supported anidentical phylogenetic position for birds withinthe maniraptoran coelurosaur theropods.

Osteological evidence of the theropod ances-try of birds—that is, derived characters sharedby birds and some portion of theropod dino-saurs—comes from essentially all parts of thebody. The evidence has been well reviewed(e.g. Witmer 1991; Padian and Chiappe 1997,1998; Sumida and Brochu 2000), but it is worth-while to summarize here the extent and detailof the evidence explicitly for ornithologists.

Theropod dinosaurs were primitively biped-al, but there were several evolutionary trends intheropod morphology as they evolved more ef-ficient bipedal locomotion (Gatesy 1990, 1991,1995; Gatesy and Middleton 1997; Farlow et al.2000; Hutchinson 2000a, b; Hutchinson and Ga-tesy 2000). Notably, the origins and insertionsof muscles that move the hindlimbs changedradically, leaving observable traces on bones asthey evolved. For example, in alligators andearly theropods, the M. caudofemoralis longus

January 2002] 3Perspectives in Ornithology

FIG. 1. A phylogeny of the theropod origin of birds based on Sereno (1999) with several new taxa added(Xu et al. 1999a, 1999b, 2000; Ji et al. 2001), and a phylogenetic hypothesis for the origin of feathers. Theornithischian and sauropod dinosaurs are the two immediate sister groups to the theropod dinosaurs. Taxawith feathers are labeled *, and taxa demonstrated to have fully modern, pennaceous feathers are labeled **.The lineages in which the first feathers and fully pennaceous feathers are most parsimoniously hypothesizedto have evolved are labeled * and **, respectively.

originates far out on the tail and inserts on thefourth trocanter down the shaft of the femur;gradually, the origin of the muscle was dis-placed toward the base of the tail, and its in-sertion on the femur was reduced. In modernbirds, that primitively important archosaurianlocomotory muscle is reduced to a thin slip, oneof those numerous curious, vestigial pieces ofavian anatomy. Within theropods, the tailshortened, the basal portion of the tail shortedeven further, and the distal elements of hin-dlimbs elongated. The fibula became a thin

splint in dromaeosaurs and birds. In the ankle,the ascending process of the astragalus becamelarger and evolved into the avian pretibial bone(Gauthier 1986; Rieppel 1993; Padian andChiappe 1997, 1998). In the foot, the fifth toewas reduced to a single metatarsal, and the firsttoe was reduced and raised off the ground,leaving a functionally tridactyl foot. The firsttoe subsequently reevolved a lower positionwithin birds with the evolution of the graspinghallux. The avian pelvis also shows a numberof additional derived characters revealing the-


FIG. 2. Dorsal view of the left hands of (a) Dei-nonychus antirrhopus, (b) Archaeopteryx lithographica,and (c) Nothura maculosa (Tinamidae), from Wagnerand Gauthier (1999). Notice the common phalangealformulae and the similarities in proportions andshapes of the phalanges of digit 3 shared by Deinon-ychus and Archaeopteryx. DI–III, digits 1–3; C1–3, dis-tal carpals comprising the semilunate carpal; R, ra-diale. (Reprinted with permission.)

ropod ancestry (Farlow et al. 2000, Hutchinson2000b). In the group of theropods called Tetan-urans (coelurosaurs and carnosaurs), the pubisevolved a widened end, or pubic boot. In dro-maeosaurs and birds, the pubic boot extendscaudally and the pubis evolved a retroverted,or backward directed, position. Throughouttheropods, the pubis evolved to become longerthan the ischium. In the axial skeleton, thero-pods, like birds, have pneumatic cervical ver-tebrae that are likely indications of an early airsac system. Additional synapomorphies havebeen identified in the skull, including presenceof an accessory antorbital fenestra and dorsal,caudal, and rostral tympanic recesses.

The pectoral girdle and forelimb also revealsuites of hierarchically nested morphologicalnovelties supporting the theropod origin ofbirds. In the pectoral girdle, fused clavicles, ora furcula, are now known in many theropods(contra Heilmann 1926; Chure and Madsen1996, Makovicky and Currie 1998, Norell et al.1998). The furcula is remarkably birdlike insome dromaeosaurs (Xu et al. 1999a, Burnhamet al. 2000). Also in dromaeosaurs and birds,we see the derived elongate coracoids, sternalplates (in some), and an increasingly laterallyfacing glenoid, or shoulder socket. Within thetheropods lineage leading to birds, the fore-limbs lengthened in proportion to the hind-limbs, and the hand elongated in relation to therest of the forelimb. Also, some dromaeosaursand birds even show a prominently bowed ulna(e.g. Burnham et al. 2000)—a feature thatzooarcheologists still use to identify avian ul-nae in human middens.

The wrist of higher coelurosaurs is charac-terized by the fused distal carpals 1 and 2 (Gau-thier 1986; Padian and Chiappe 1997, 1998). InArchaeopteryx, dromaeosaurs, and even ovirap-torans and troodontids, those fused distal car-pals form a crescent-shaped bone generallycalled the semilunate carpal (Ostrom 1974;Gauthier 1986; Gauthier et al. 1988; Padian andChiappe 1997, 1998). It is universally agreedthat the function of that exceptional structure isto allow the wrists to swivel sideways. Thatfeature was the character that first led Ostrom(1974) to question 50 years of orthodoxy and ar-gue for the theropod origin of birds.

Theropods exhibit a simultaneous trend to-ward loss of digits and the evolution of a grasp-ing hand. Primitively, dinosaurs have five fin-

gers. The outer two digits, number four andfive, are reduced but present in Herrerasaurus(variously hypothesized to be a basal dinosaur,basal Saurischian dinosaur, or basal theropod).Subsequently, in theropods the outer digits ofthe hand are completely lost, leaving digits 1,2, and 3, as in birds. The fingers of dromaeo-saurs and Archaeopteryx also have the samephalangeal formula (number of phalanges ineach digit); the first, second, and third digitshave two, three, and four phalanges,respectively.

Theropods also share some remarkable, de-rived phalangeal proportion and shapes withArchaeopteryx (Wagner and Gauthier 1999, Hop-son 2001). The second digit is longest in thero-pods and birds despite its fewer phalanges. In afew well-known dromaeosaurs (e.g. Deinony-chus, Bambiraptor, and Sinornithosaurus) and inArchaeopteryx, the middle two phalanges in digit3 are substantially shorter than either the first orfourth (Fig. 2). Further, those shorter, middlephalanges are twisted along their axes, so thatthe third digit does not flex parallel to the oth-


ers, but twists inward toward the center of thehand (Wagner and Gauthier 1999, Hopson 2001).That unique and bizarre morphology gives riseto the curious curled position of digit 3 in manyArchaeopteryx specimens and related dromaeo-saurs (e.g. Sinornithosaurus; Xu et al. 1999a).These new observations demonstrate that Heil-mann’s (1926) reconstruction of the hand of Ar-chaeopteryx with digit 3 lying nicely parallel todigit 2 is incorrect. Digit 3 of Archaeopteryxmoved independently of digit 2, maintaining agrasping function underneath the wing feathersas many specimens of Archaeopteryx show. A re-vised reconstruction of the hand of Archaeopter-yx (Fig. 2) also explains the apparently anoma-lous insertion of the remiges on digit 2 (themiddle digit) instead of digit 3, which would bethe trailing edge of the wing.

In summary, osteological synapomorphies ofbirds and theropod dinosaurs come from thedetailed similarities of many parts of thebody—head to toe, tip to tail. As the recent de-bate over the phylogenetic position of Monon-ychus (Zhou 1995, Chiappe et al. 1996, Sereno1999) and Caudipteryx (Ji et al. 1998, Feduccia1999b, Jones et al. 2000a, Zhou 2000, Zhou andWang 2000, Zhou et al. 2000) makes clear, it isincreasingly difficult even to distinguish a birdfrom other theropods. This summary has al-most excluded consideration of the newest,most exciting, and perhaps most compellingfossils finds from the Yixian formation ofLiaoning, China. The explosion of critical spec-imens from those deposits in the last few yearshas revolutionized the quality and quantity ofevidence bearing on the origin and early evo-lution of birds (Stokstad 2001). Those speci-mens include conclusive evidence of the stron-gest possible bird–theropod synapomorphy—completely modern feathers (see below)—andthe oldest, most birdlike dromaeosaurs.

CRITICISMS OF THE THEROPOD ORIGIN OF BIRDS

Despite the wealth of and increasingstrength of the evidence, the theropod hypoth-esis of the origin of birds has received unre-lenting criticism for more than two decades.These criticisms can be grouped in several clas-ses: general critiques of phylogenetic methods,criticisms of the validity and homology of spe-cific characters, temporal disparity between theavian and theropod radiations, and a priori ar-

guments about functional and physiologicalplausibility. Although critiques have been ef-fectively countered in the literature many times(e.g. Witmer 1991; Padian and Chiappe 1997,1998; Sumida and Brochu 2000), criticisms haveremained largely unchanged (e.g. Feduccia1999a, b; Dodson 2000).

Criticisms of phylogenetic methods. Since Gau-thier (1986), the bird-origin debate has reallybeen about methods of analysis. Two alterna-tives are represented: phylogenetic systematics,in which explicit historical hypotheses of rela-tionships among monophyletic groups are pro-posed based on hypothesized shared derivedcharacters; and traditional eclectic narrativemethods, that have remained essentially un-changed since Heilmann (1926), in which noexplicit analytical method is used, and no at-tempts are made to actually document the phy-logenetic history of lineages related to birds.Now, phylogenetics is universally recognizedin systematics and evolutionary biology, andeven by U.S. courts (e.g. in cases of criminalHIV infection; Vogel 1997). But, critics of thetheropod origin of birds have been a singularexception to that nearly universal intellectualtrend. Steadfastly they have maintained thatphylogenetics cannot be relied upon to solvethe question of the origin of birds (e.g. Feduccia1999b, Dodson 2000).

A few explicit alternative phylogenetic hy-potheses to the theropod theory have beenproposed in recent decades—that birds are re-lated to crocodilians (Walker 1972; Whetstoneand Martin 1981; Martin 1983a, b), or that birdsare related to the early archosaur Euparkeria(Welman 1995). The crocodile hypothesis hasbeen abandoned in recent years after scrutinyof the details, and several phylogenetic analy-ses have failed to support Euparkeria as a closeavian relative (Sumida and Brochu 2000). Sev-eral early archosaurs or archosaurimorphs havealso been proposed as candidate ‘‘thecodontrelatives’’ of birds (e.g. Longisquama, Scleromo-chlus, and Megalancosaurus), but not in the strictphylogenetic sense of exclusive, shared ances-try. Rather, it is usually stated that birds mayhave evolved through a similar morphological‘‘stage’’ (e.g. Jones et al. 2001). Because thoseproposals are lacking in supporting details,they do not constitute credible alternative sistertaxa. All detailed analyses of the array of alter-native archosaurian sister-groups of birds have


demonstrated than none has any substantialsupport (Sumida and Brochu 2000). The mostrecent proposal of feathers in the Triassic Lon-gisquama (Jones et al. 2000b) received immedi-ate criticisms on numerous grounds (Reisz andSues 2000, Prum 2001, Unwin and Benton 2001,Prum and Brush 2002). As Sumida and Brochu(2000) point out, no alternative has any morethan a few superficially birdlike features; butphylogenetic analyses have already identified agroup with numerous hierarchically distribut-ed, derived morphological features sharedwith birds—theropod dinosaurs.

Criticisms of the characters. A frequent criti-cism of the evidence in support of the theropodorigin of birds has been ‘‘garbage in, garbageout.’’ The implication is that derived characterstates hypothesized to be shared by birds andtheropods are too dissimilar, incorrectly ho-mologized, or functionally important andtherefore too convergent to be historically in-formative (e.g. see Martin et al. 1980, Martinand Stewart 1985, Feduccia 1999b).

Characters are often rejected on the basis ofsome preconceived notion about the evolution-ary process (Padian 2001). For example, it is hy-pothesized that birds must have evolved flightfrom trees, so their ancestors must have beenarboreal. Thus, bipedality of terrestrial thero-pods and birds must be convergent, and allhindlimb, pelvis, and tail characters can be dis-counted (Feduccia 1999b). However, in parallelwith the universal adoption of phylogeneticmethods in systematics, there has been anequivalent recognition that it is essential to es-tablish a phylogenetic pattern before (e.g. Lau-der 1990, Larson and Losos 1996, Lauder andRose 1996), or independently of (e.g Padian2001), the analysis of functional and macroevo-lutionary process. The ability to merely con-ceive of two features as convergent is consid-ered by critics to be sufficient criteria to rejecta proposed synapomorphy completely: for ex-ample Feduccia and Martin’s (1998) critique ofthe Velociraptor wishbone. However, only a phy-logenetic analysis that includes all proposedcharacters and taxa can resolve whether char-acters are phylogenetically informative. To re-ject a hypothesis of homology, it is necessary toshow that the proposed similarities evolvedconvergently within a phylogenetic analysis in-cluding other phylogenetically informativecharacters (Patterson 1982, Pinna 1991).

Ironically, rejection of nearly any aspect ofavian anatomy as phylogenetically informativewill undermine any future attempts to supportan alternative hypothesis. Thus, if the furculashared by many higher theropods and birdscan be ignored as uninformative, how can oneargue that the presence of furcula in Megalan-cosaurus or Longisquama is somehow a validcharacter? Critics of the theropod hypothesisare predictably unconcerned about that prob-lem because they do not actually intend to es-tablish a sister group to birds.

In a few cases, valid criticisms of the characterdata have been made, but, tellingly, those criti-cisms have actually strengthened the supportfor the theropod hypothesis. For example, Os-trom (1974) originally homologized the semilu-nate carpal with the avian radiale, but Martin(1983a, b) pointed out that homology could notbe correct because the semilunate carpal of Ar-chaeopteryx becomes fused within the carpome-tacarpus in higher birds, and that the radiale isa proximal carpal(s). Following Martin’s obser-vation that the semilunate carpal was composedof distal carpals, Padian and Chiappe (1997,1998) recognized that the fusion of distal carpals1 and 2 actually evolved much earlier in thero-pods than previously recognized by Ostrom(1974). Subsequently, the semilunate shape ofthat novel element was derived in the commonancestor of maniraptorans. A reanalysis basedon Martin’s criticism provides an expanded his-torical context for the explanation of both the or-igin of the novel element and subsequent evo-lution of its unique semilunate shape.

If ornithologists want to evaluate the char-acter analysis methods of some vocal critics ofthe theropod hypothesis, a good example canbe found in the quasi-phylogenetic hypothesisof early bird phylogeny proposed by LarryMartin, Alan Feduccia, and colleagues (Hou etal. 1996). Those authors proposed that Archae-opteryx and Confuciusornis were the sistergroup to enantiornithine birds, and that Liaon-ingornis and Chaoyangia are the sister group toall other birds, including modern birds. How-ever, because enantiornithines had many ad-vanced flight features found in modern birds,that hypothesis requires the convergent evolu-tion of the keeled sternum, the strut-like cora-coid, the tarsometatarsus, the shortened tail,and the pygostyle. Curiously, the modern birdsappear in their published phylogeny but not in


the unpublished data set or analysis on whichit is based (Hou et al. 1996; supplemental ma-terials can be found online, see Acknowledge-ments). The authors decided that the tarsome-tarsi in various birds were different enough toconclude that all of those characters are conver-gent within birds. Needless to say, most orni-thologists would have difficulty in acceptingthat all those features had evolved convergentlyin birds. Numerous phylogenetic analyses (e.g.Chiappe 1995, Chiappe et al. 1999) have shownthat enantiornithines are phylogenetically closerto extant birds than are Archaeopteryx or Confu-ciusornis, supporting a single origin of those ad-vanced flight features and rejecting Hou et al.‘s(1996) and Martin’s (1983b) hypothesis of tar-sometatarsus evolution. However, Hou et al.(1996) demonstrates the advantages of present-ing an explicit hypothesis, and documents an or-nithological example of the type of characteranalysis promoted by critics of the theropod hy-pothesis. It can be hoped that these and othercritics of the theropod hypothesis will soon at-tempt a phylogenetic analysis of the nonthero-pod origin of birds that can be scrutinized aseasily.

1–2–3 versus 2–3–4. One criticism of the the-ropod hypothesis deserves detailed consider-ation because it has frequently been cited as thebiggest obstacle to the theropod origin of birds.The avian hand has three digits. On the basisof phylogenetic analyses of digit reduction indinosaurs, theropods are universally recog-nized as having digits 1–2–3 (Hinchliffe 1985;Wellnhofer 1985; Burke and Feduccia 1997; Pa-dian and Chiappe 1997, 1998; Feduccia 1999a,b; Wagner and Gauthier 1999). In contrast, de-velopmental biologists have traditionally re-ferred to the digits of the hand in birds as 2–3–4 (Hinchliffe 1985; Burke and Feduccia 1997;Feduccia 1999a, b; Wagner and Gauthier 1999),because the first cartilage condensation to de-velop in the hand (and foot) of most amniotesbecomes distal carpal 4 and metacarpal 4, andthe most posterior digit in the avian hand ul-timately develops above this first condensation(Hinchliffe 1985, Burke and Feduccia 1997).Thus, the traditional developmental hypothesisis that the digit that develops above metacarpal4 is digit 4 because its identity is determined byits position. Therefore, fingers of birds must bedigits 2–3–4, they cannot be homologous withthose of theropods, and all similarities in pha-

langeal formula, proportions, shape, and func-tion shared by fingers of birds and theropodsmust be convergent. That conclusion ‘‘is basedupon classical homology and reliance on theprinciples of developmental position and con-nections’’ (Feduccia 1999b:385). Of course, suchreasoning only further raises the question ofhow the digits of theropod hands could havedeveloped in the absence of the essential fourthmetacarpal developmental axis, but the extinc-tion of nonavian theropods has convenientlyprevented anyone from acquiring those data.

Wagner and Gauthier (1999) proposed the‘‘frame-shift’’ hypothesis as a solution to thisapparent conflict. Essentially, they hypothesizedthat the theropod hand evolved to develop digits1–2–3 in positions 2–3–4. Comparing the frame-shift hypothesis to Lysenkoism, cold fusion, anda ‘‘cladistic jihad,’’ Feduccia (1999a) suggestedthat Wagner and Gauthier (1999) were denyingthe developmental facts to maintain the credi-bility of the theropod hypothesis. Recently,however, Dahn and Fallon (2000) published a se-ries of experiments on development of chick hin-dlimb digits that demonstrate that amniote digitidentity is not an inherent property of the digitprimordia or their positions. Rather, identity ofthe developing digit primordia is initially un-specified despite their positions. Instead, digitidentity is determined by the interactions be-tween the digit primordia and gradients of pat-tern formation genes (e.g. bone morphogeneticproteins, or ‘‘BMPs’’) in the interdigital meso-derm that surrounds the digit primordia early indevelopment (Dahn and Fallon 2000). By trans-planting digit primordia and the interdigitalmesoderm within and among chick feet, they ex-perimentally created homeotic transformations(i.e. changes to the identity of any digit) andgrew any digit in any position (Fig. 3). Further,by experimentally manipulating BMP levels inthe interdigital mesoderm, Dahn and Fallon(2000) could anteriorize or posteriorize all digitsof the hand (as hypothesized by the frame-shifthypothesis; Fig. 3). They were even able to pre-dictably grow digits with extreme phalangealformulae that do not occur among known ar-chosaurs. Interestingly, as developmental biolo-gists, R. D. Dahn and J. F. Fallon (pers. comm.)were entirely uninvolved with the paleontolog-ical and systematic debate on the homology ofdigits of the avian hand.


FIG. 3. Control and experimental homeotic transformations of digit identity in the foot of chicks (Gallusgallus) from Dahn and Fallon (2000). (A) The standard phalangeal formula with digits1–4 having 2–5 pha-langes, respectively. (B) Homeotic transformation of of all digit identities produced by beads (dots) withSonic Hedgehog protein between digits. Each digit has an additional phalanx, typical of posteriorization ofdigit identity. (C) Homeotic transformation of the identity of digit 2 to a digit 1 produced by a bead (dot)with Noggin protein between digits 2 and 3. The transformation of digit 2 to1 is accomplished by the loss ofa phalanx, or an anteriorization of digit identity. (Reprinted with permission.)

Dahn and Fallon’s (2000) work provides mo-lecular developmental evidence supporting theplausibility of the frame-shift hypothesis (Galis2001). It is entirely plausible for theropods tohave evolved changes in patterns of BMP ex-pression in the developing hand that wouldlead to a frame-shift in digit identity. Further-more, Dahn and Fallon’s (2000) data falsify theprimary assumption of 2–3–4 hypothesis: thatthe conserved patterns of metacarpal develop-ment within the hand dictate digit identity. Farfrom ‘‘accommodating the cladogram’’ (Fed-uccia 1999a), Wagner and Gauthier (1999) madea bold prediction that the developmental un-derstanding of digit identity must be incom-plete. Dahn and Fallon (2000) independentlydemonstrated that this prediction was correct.Although many details remain to be investi-gated, it is now clear that there is no conflict be-tween the theropod hypothesis of bird originsand the facts of developmental biology.

‘‘Temporal paradox’’. Another criticism of thetheropod hypothesis is the supposed ‘‘tempo-ral paradox’’—the notion that theropod diver-sity is too young to be phylogenetically closelyrelated to birds. The objection has been thatfossils presumed to be closest to birds are toolate in time compared to the first bird, Archae-opteryx, approximately 148 my old (Sereno1997). Many dromaeosaurs, ornithomimid, ovi-

raptoran, and other theropod fossils includedin the hypothesis are best known from the LateCretaceous, or about 80 Ma, but many areknown from much earlier. The notion of a tem-poral paradox is based on several fundamentalmisconceptions about paleontology and evo-lutionary biology (Padian and Chiappe 1998),and by misrepresentation of the evidence (Pa-dian and Chiappe 1998, Brochu and Norell2000).

The first misconception is thinking purely interms of prephylogenetic ancestor–descendantrelationships. For example, A. Feduccia has of-ten repeated that birds cannot be related to the-ropod dinosaurs because ‘‘you can’t be yourown grandmother.’’ However, phylogenetic hy-potheses are statements about the history ofshared ancestry among lineages. The theropodhypothesis does not imply that Deinonychus, orany other Late Cretaceous dromaeosaur, is ac-tually ancestral to birds. Rather, the theropodhypothesis proposes that those organismsshared an exclusive common ancestor. Further,Feduccia (1999b:90) has stated that ‘‘one couldinterpret the temporal evidence as indicatingthat birds and dinosaurs are indeed examplesof convergent evolution.’’ Such reasoning im-plies that distribution of stochastic samples inpaleontological time can be used to reject aphylogenetic analysis based on many detailed


characters that are directly observable. Lastly,critics imply that such temporal disjunctionsare rare or unexpected. But, as Padian andChiappe (1998) point out, the fossil record ofmonotremes goes back less than 20 Ma, where-as the fossil record of therian mammals goesback 100 Ma. Yet, no one could credibly arguethat this 80 my temporal disjunction could af-fect our confidence that monotremes are the sis-ter group to all other extant mammals.

The magnitude of the supposed temporalparadox has also been greatly and repeatedlyexaggerated. Recently, Feduccia and Martin(1998), Feduccia (1999b), and Dodson (2000) allcharacterized the temporal disjunction be-tween Archaeopteryx and dromaeosaurs as be-tween 60–80 my. Those authors have plainly ig-nored fragmentary fossils indicating existenceof dromaeosaurs in the Late Jurassic (Jensonand Padian 1989). Furthermore, at least threetaxa of basal dromaeosaurs are now knownfrom the 124 Ma old Yixian formation of Liaon-ing, China (Xu et al. 1999b, 2000, 2001; Ji et al.2001) which is only 24 my younger than Ar-chaeopteryx. Not only are these new taxa theoldest, well-known dromaeosaurs, but they arethe most birdlike theropods in many features,including their small size and obvious feathers.If a temporal paradox ever existed, it has beensubstantially reduced to between 0 and 24 my.

Stated phylogenetically, the temporal para-dox assumes that sister taxa should have thesame data of origin in the fossil record. That ex-pectation is unrealistic given the inherentpatchiness of the paleontological record. Forexample, the handful of specimens of Archae-opteryx are themselves amazing chronologicaloutliers given the lack of any other known Ju-rassic birds. Until very recent discoveries fromthe Early Cretaceous in China (Stokstad 2001),even very few Early Cretaceous birds wereknown (Martin 1983a). Of course, the temporaldisjunction between Archaeopteryx and otherbirds does not lead us to question the mono-phyly of birds. Furthermore, Brochu and Norell(2000) have demonstrated that the ‘‘temporalparadox’’ is equivalent or even greater for allproposed alternatives to the theropod hypoth-esis of avian origins.

Functional and physiological criticisms. An-other common method used to criticize the the-ropod hypothesis is to make a priori assump-tions about which functional or physiological

transitions are evolutionarily likely or impos-sible, and then use that ‘‘knowledge’’ of howevolution works to reject phylogenetic analysesbased on a wealth of character evidence. Ex-amples include numerous analyses of the ori-gin of avian flight (e.g. Feduccia 1985, Tarsitano1985), lung ventilation (Ruben et al. 1997), andhomeothermy and growth rates (Ruben andJones 2000). These particular issues have beenrebutted well elsewhere (Padian and Chiappe1998, Padian et al. 2001, Perry 2001).

IMPLICATIONS OF THE THEROPOD ORIGIN

OF BIRDS

Is the theropod origin of birds relevant to thebiology of modern birds? Advances in applyingphylogenetic methods to many questions inecology and behavior have helped demonstratethe relevance of phylogenetic history of manyaspects of avian biology, but many ornitholo-gists may think that those ancient events arenot important. Actually, I think that the impli-cations of the theropod origin of birds to the bi-ology of modern birds are many, broad, andvaried, and that the theropod origin should befundamental to how we think about and studyavian biology. Here, I will review a series ofexamples.

Feathers. Possesion of feathers has been con-sidered as synonymous with birds by humancultures essentially forever (with exceptions forangels; Pinna 1991). Recent paleontologicaldiscoveries have demonstrated that feathersoriginated and diversified in theropod dino-saurs before the origin of birds and of flight(Chen et al. 1998; Ji et al. 1998, 2001; Schweitzeret al. 1999; Sereno 1999; Xu et al. 1999a, b, 2000,2001; Padian 2001; Sues 2001; Prum and Brush2002). I discuss this topic here because I wantto emphasize the implication of these data forhow we think about and how we need to re-think avian biology (see Prum and Brush 2002for thorough review).

In the last five years, the Early CretaceousYixian formation of China and the Late Creta-ceous of Mongolia have produced fossils ofeight nonavian theropod dinosaurs that havefilamentous integumental appendages thathave been hypothesized to be homologous withavian feathers: Sinosauropteryx (Chen et al.1998), Shuvuuia (Schweitzer et al. 1999), Bei-piaosaurus (Xu et al. 1999b), Caudipteryx (Ji et al.


FIG. 4. Phylogenetic hypothesis of the evolution of pelvis shape and the origins of locomotor muscles inthe reptile lineage leading to birds, from Hutchinson (2000b). (Reprinted with permission.)

1998), Protarchaeopteryx (Ji et al. 1998), Sinor-nithosaurus (Xu et al. 1999a, 2001), Microraptor(Xu et al. 2000), and an unnamed basal dro-maeosaur (Ji et al. 2001). One of those taxa,Caudipteryx, has indisputable evidence ofbranched, pennaceous feathers (Ji et al. 1998),and repeated phylogenetic analyses based onnumerous characters have demonstrated thatCaudipteryx is a basal oviraptoran dinosaur(Sereno 1999, Zhou 2000, Zhou and Wang 2000,Zhou et al. 2000). Critics of the theropod hy-pothesis have called that taxon a secondarilyflightless bird based only on its body propor-tions (Jones et al. 2000a), or brief discussion ofa few characters in absence of any explicit anal-ysis of the character data (e.g. Martin and Czer-kas 2000). Sinosauropteryx is a basal coelurosaurwith small (about 5–6 mm) integumentary ap-pendages that are apparently cylindrical, andmay also be branched in some fashion (Chen etal. 1998). Beipiaosaurus (a therizinosaur), andSinornithosaurus, Microraptor, and another un-named taxon (all basal dromaeosaurs) all havelong filamentous integumentary appendagesthat are diverse in size and structure (Xu et al.1999a, b, 2000, 2001; Ji et al. 2001). Detailedanalyses of the structure of integumentary ap-pendages of Sinornithosaurus have demonstrat-

ed that they share three unique features withavian feathers: multiple filament structure, bas-al branching, and serial branching (Fig. 4; Xu etal. 2001). Subsequently, the integumentary ap-pendages of an unnamed but closely relateddromaeosaur taxon further document a vane ofparallel barbs running at an acute angle in ex-actly the conformation of a pennaceous feather(Ji et al. 2001). Those fossil structures are es-sentially indistinguishable from the contourfeathers of confuciusornithine and enantiorni-thine birds preserved in the same strata.

New theropod integumental structures havebeen repeatedly dismissed as connective tis-sues, such as frayed collagen fibers or ossifiedtendons (Feduccia 1999a, b; Martin and Czer-kas 2000; Ruben and Jones 2000). But none ofthose critics have explained why a therizino-saur would have 70 mm collagen filamentshanging of the trailing edge of its ulna in theexact position of avian remiges (Xu et al.1999b); why a dromaeosaur (Sinornithosaurus)would have a 35 mm ossified tendon emergingfrom the tip of its snout (Xu et al. 2001); or whycollagen fibers would be indistinguishablefrom feathers preserved in the same rock? Fur-ther, there is now paleobiochemical evidencethat the filamentous integumentary append-


ages of Shuvuuia, an alvarezsaurid related tothe ornithomimid theropods, are composed ofb-keratin (Schweitzer et al. 1999) which occursonly in the epidermis.

The theropod origin of feathers (Padian 2001,Sues 2001, Prum and Brush 2002) has tremen-dous implications for avian biology. Possessionof feathers is no longer synonymous with birds,nor did feathers evolve for flight. Feathers orig-inated and diversified in terrestrial theropoddinosaurs, and were only subsequently co-optedto function in flight by birds (Prum and Brush2002). Feathers can no longer be considered thereason why birds survived the Cretaceous–Ter-tiary boundary, because numerous lineages offeathered theropods went extinct at this time.Why did birds survive? That question can beaddressed in future research without feathersas a consideration.

Flight. The theropod origin of birds andfeathers has important implications for the evo-lution of avian flight. The origin of birds, feath-ers, and avian flight are the central trinity of ear-ly avian evolution. Unfortunately, these threequestions are frequently addressed as interde-pendent and correlated hypotheses. Critics ofthe theropod hypotheses usually advocate a the-codont origin of birds, an aerodynamic origin offeathers, and an arboreal origin of flight (Fed-uccia 1999b). In contrast, supporters of the the-ropod hypothesis have usually advocated athermoregulatory origin of feathers and a ter-restrial origin of flight (Ostrom 1974). Unfortu-nately, treating those hypotheses as necessarilyinterdependent is scientifically constraining, un-productive, and unnecessary. There is nothingabout the theropod origin of birds that excludesthe possibility that flight could have evolvedfrom tress (e.g. Chatterjee 1997). However, thetheropod origin of birds makes it clear that an-cestors of birds were cursorial bipeds, and thatmany of the morphological features that wereultimately co-opted, or exapted (Gould andVrba 1982), in the evolution of the wing and theflight stroke evolved in a terrestrial context for apurpose other than flight (Gauthier and Padian1985; Padian and Chiappe 1997, 1998; Padian2001). Those characters include numerous fea-tures of the forelimb, shoulder girdle, wrist, andmanus that allowed birds to evolve a flightstroke from a prey grasping movement.

Rayner (1985) and others have pointed outthat flying at faster speeds requires a simpler

wing ‘‘gait’’ (i.e. a continous wing vortex), andfewer morphological specializations than doesflying at slower speeds or taking off from theground (which require a ring-vortex). This factplaces a substantial functional challenge tohow a terrestrial biped could have evolvedflight purely from the ground. However, Bur-gers and Chiappe (1999) recently pointed outthat previous models had ignored the fact thatflapping feathered wings while running willconsiderably increase the ground speed beforetake off. Consequently, they hypothesize Ar-chaeopteryx and the maniraptoran ancestors ofall birds could have become airborne by flap-ping and running simultaneously. We maynever have definitive evidence of the ecologicalcontext—arboreal or terrestrial—of the originof flight in theropods, but it is clear from cur-rent evidence that the major components of theflight stroke had already evolved in bipedaltheropods in a wholly terrestrial context (Gau-thier and Padian 1985; Padian and Chiappe1997, 1998).

Terrestrial locomotion. The theropod originof birds also has other important implicationsfor the evolution of avian terrestrial locomo-tion. Gatesy and Dial (1996) observed that theevolution of avian flight required decoupling ofthe coordinated forelimb and hindlimb move-ments that are a primitive feature of reptilianlocomotion, and the evolution of a novel neu-rological motor coupling of forelimb and tailmovements. Because bipedal locomotion wasprimitive to theropods, forelimbs and hin-dlimb movements had already been evolution-arily decoupled within that lineage. Thus, asflight evolved in birds, new neuromuscular as-sociations could evolve between wing and tailfunction required for controlled flight withoutcompromising terrestrial locomotion. Gatesyand Dial’s (1996) observations of avian loco-motor modules underscores another challengeto the traditional arboreal theory of the originof flight, which proposes that avian flightevolved directly from lizardlike quadrapedalarboreal ancestors.

Steve Gatesy and colleagues (Gatesy 1990,1991, 1995; Gatesy and Dial 1996; Gatesy andMiddleton 1997; Hutchinson and Gatesy 2000)have done a number of comparative analyses ofthe evolution of terrestrial locomotion in birdsand other theropods. This body of work has un-derscored the functional continuity between


birds and other theropods, while also identi-fying derived features of avian locomotion andplacing them in an historical context. For ex-ample, John Hutchinson (2000a, b) has donecomparative phylogenetic analyses of the evo-lution of the shapes of the theropod and avianpelvis and femur; the origins, insertions, andsizes of various hindlimb muscles; and the lo-comotor consequences of those changes (Fig.4). He concludes that many muscular featuresthought to be unique to birds can be under-stood historically as the extreme in a continu-um of morphological character state evolution.Morphologically and functionally, extant birdsare much less distinct, and therefore more eas-ily understood, in the context of their theropodorigin. This groundbreaking body of work byGatesy, Hutchinson, and colleagues demon-strates vividly how the theropod hypothesis ofavian origins provides an historical context forunderstanding extant avian diversity.

Nesting biology and clutch size. Perhaps fewfeatures of avian biology have been as wellstudied as reproductive behavior and ecology.Yet it is little appreciated that fundamental as-pects of avian reproductive biology evolvedduring early archosaurian and theropod ances-try. For example, birds are often consideredunique among vertebrates for the extent andubiquity of parental care. It is easy to see, how-ever, that extensive parental care is primitive toarchosaurs. Crocodylians have obligatory nestbuilding, nest defense, and extensive post-hatching parental care. Young pterosaurs wereincapable of flight during early growth, andmust have received extensive parental care inearly life (Ricqles et al. 2000). The evidence ofnesting and parental care in ornithischian, sau-ropod, and theropod dinosaurs is extensive(Currie and Padian 1997). Thus, this funda-mental feature of avian biology is not exclu-sively avian, but essentially archosaurian.

The most dramatic evidence of similarity ofpaternal care in birds and other theropodscomes from the nests of Oviraptor found inMongolia (Clark et al. 1999). This striking fossilshows an Oviraptor (erroneously believed to bestealing eggs when first described!) lying ontop of a terrestrial clutch of eggs in a perfectlyfossilized brooding posture. Unlike the primi-tive archosaurian condition found in croco-diles, Oviraptor did not place vegetation overthe top of the nest. The forelimbs of the brood-

ing individual are held at the sides but distinct-ly apart from the body as if covering the rest ofthe clutch with its wing feathers. Thus, anothereminently avian feature—brooding—likelyalso had an origin somewhere in theropod di-nosaurs prior to the evolution of birds.

David Varricchio and colleagues (Varricchioet al. 1999) have been conducting research onthe nest of Troodon formosus that reveal somemore remarkably birdlike details to theropodreproduction. Troodon and other theropodsprobably laid pairs of eggs, instead of singleeggs as in most birds, because they still hadtwo ovaries. The 24 eggs in each clutch werelaid in pairs instead of all at once, which is theprimitive condition of crocodylians and mostother reptiles. Thus, the clutch appears to becomposed over a series of days, and anotherdistinct feature of avian reproduction appearsto have originated in the theropod ancestors ofbirds. The typical avian traits of having onefunctional ovary and laying single eggs per dayare apparently derived in birds. So, serial com-position of the clutch was not a weight-reduc-tion adaptation for flight because it apparentlyevolved in theropods before the origin of flight.

Another interesting feature of the Troodonnests is their clutch size. One of the fundamen-tal limitations on the size of a clutch laid overa series of days is the time it takes for an un-incubated egg to spoil. If a clutch takes toomany days to complete, then the first eggs laidwill begin to spoil before the entire clutch is in-cubated. Like birds, Troodon likely delayedbrooding until the entire clutch was completeto synchronize hatching. Although the Troodonclutch size was 24, it was likely laid over ;12days, corresponding to an avian clutch size of12 eggs. So, it is possible that one of the pri-mary determinants of clutch size in precocialbirds has persisted since the origin of serialclutch assembly in the theropod ancestors ofbirds.

Growth and metabolic rates. Avian growthand metabolic rates are of great interests toecologists and physiologists. Recently, Padianet al. (2001) reviewed the evidence of dinosaurgrowth rates and metabolic rates inferred frompaleohistology. A conservative conclusion isthat dinosaurs evolved substantially highergrowth rates than other archosaurs and rep-tiles, further substantiating the hypothesis thatdinosaurs were not typical ectotherms. The


evolution of growth rates in early birds is alsointerestingly complex. Some lineages appear toshow conspicuously slower growth rates thanwere typical of their theropod ancestors (e.g.confuciusornithine and enantiornithine birds).Padian et al. (2001) hypothesize that this mayhave been associated with the initial evolutionof small size in early birds. Subsequently,growth rates increased again in modern birds.As with many other features of avian biology,investigation of the theropod context of avianorigins establishes that many characteristicspreviously thought to be unique to birds can beunderstood to have evolved in their more an-cient avian ancestors.

CONCLUSIONS

The theropod hypothesis of the origin ofbirds is the only phylogenetically explicit hy-pothesis available for the relationships of birdsto other archosaurs. Shared derived anatomicalcharacters in support of this hypothesis comefrom all parts of the skeleton, and recent fossilevidence also documents that fully modern,pennaceous feathers, and many birdlike repro-ductive behaviors evolved in theropod dino-saurs before the origin of birds. The theropodorigin of birds has important implications forresearch and teaching in all fields of ornithol-ogy. The theropod hypothesis of the origin ofbirds has already generated startling new pre-dictions about other fields of biology that havebeen confirmed by independent research—forexample the development of digit identity inamniotes. The theropod hypothesis impliesthat numerous archetypical avian featuresevolved in theropod dinosaurs before the ori-gin of birds or flight, including feathers, hollowbones, the wishbone, and likely air sacs, brood-ing, and serial composition of the clutch. Phy-logenetic analyses of morphology further dem-onstrate that the evolution of avian anatomycan be coherently understood in terms of thetheropod ancestry of birds (e.g. Hutchinson2000a, b). These discoveries have not only ex-panded our knowledge of early bird evolution(Chiappe 1995, Padian and Chiappe 1998), butthey challenge ornithologists to revise our di-agnosis of what a bird is.

Our understanding the relevance of thero-pod origins to ornithology is just beginning.Numerous insights await future research. How

can ornithologists participate? First, the the-ropod origin of birds and general dinosaur bi-ology should be taught in all introductory or-nithology courses. The Encyclopedia of Dinosaurs(Currie and Padian 1997) is an excellent placeto start for supplemental material. (Interestedornithologists can also contact the author forsample lecture notes.) Basic dinosaur biologyand the theropod origin of birds should be in-corporated in all future ornithology textbooks:there is not a single chapter of a standard or-nithological text that could not include addi-tional insights on avian biology based on theirtheropod origin. But textbooks are based on thescientific literature. It will be important for or-nithologists to become broadly familiar withdinosaur diversity and apply their knowledgeof birds to the larger field of dinosaur and ar-chosaur biology. Ornithologists should developresearch partnerships with dinosaur paleon-tologists, and paleontological papers on non-avian dinosaur biology with implications forornithology should be published in ornitholog-ical journals. There are now many examples ofresearch that bridges the narrowing gap be-tween birds and other dinosaurs and genuinelycontribute to ornithological knowledge (e.g.Gatesy and Middleton 1997; Wagner and Gau-thier 1999; Hutchinson 2000a, b).

Until any credible alternative is proposed, itis time to abandon debate on the theropod or-igin of birds, and to proceed to investigate allaspects of the biology of birds in light of theirtheropod origin. This fertile frontier of knowl-edge promises to be among the most excitingdevelopments in ornithology in the comingcentury, and ornithologists should be activelyinterested in and participating in this field. Thetime has come for our discipline to realize thatornithology is extant dinosaur biology. Orni-thology can only profit as a result.

Note added in proof: Norell et al. (2002) de-scribe a new specimen of a basal dromaeosaur(possibly a Sinornithosaurus) from the 124 Maold Yixian formation of China that has pre-served impressions of modern pennaceousfeathers including a rachis, barbs, and a planarvane. Occasional separation of barbs in thefeather vanes document presence of differenti-ated barbules as in Archaeopteryx and modernbirds. Feathers on the tip of the tail are .19 cmlong, and the beautifully preserved feathers onthe upper hindlimbs are 13.5 cm long. This lat-


est discovery conclusively demonstrates thetheropod origin of feathers and birds.

ACKNOWLEDGMENTS

I would like to thank K. Padian and T. Petersonfor helpful comments on the manuscript. I wouldalso like to thank C. Brochu, A. Brush, L. M. Chiap-pe, S. Gatesy, J. Gauthier, J. Hutchinson, K. Middle-ton, M. Norell, S. Sumida, G. Wagner, X. Xu, and Z.Zhou for additional inspiration in conversation andin print. Supplemental materials to Hou et al. 1996can be found online at http://www.sciencemag.org/feature/data/hou.shl.

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