The Auk a Quarterly Journal of Ornithology Vol

Home , Fin, Herrerasaurus, Jacques Gauthier, John Ostrom, Terrestrial locomotion

The Auk A Quarterly Journal of Ornithology Vol. 119 No. 1 January 2002

The Auk 119(1):1–17, 2002

PERSPECTIVES IN ORNITHOLOGY

WHY ORNITHOLOGISTS SHOULD CARE ABOUT THE THEROPOD ORIGIN OF BIRDS

RICHARD O. P RUM1 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- for the evolution of birds and feathers (e.g. Bock tematics and paleontology have been as divi- 1965). sively debated as the origin of birds (Padian In 1974, John Ostrom (1974) challenged the and Chiappe 1998; Feduccia 1999a, b; Dalton status quo by revitalizing the old hypothesis 2000). For most of the middle of the twentieth that birds were related to dinosaurs (Huxley century, G. Heilmann’s (1926) monumental 1868, 1870; Williston 1879) or, more specifically, analysis of the topic reigned unchallenged. to a group of the meat-eating theropod dino- Heilmann established definitively that birds saurs, represented by Deinonychus which he are members of the Archosauria (the large rep- had recently described. Jacques Gauthier (1986) tilian clade that also includes crocodiles, ptero- subsequently confirmed that birds were a lin- saurs, and dinosaurs). But Heilmann was un- eage of theropod dinosaurs most closely relat- able to accept the voluminous evidence he ed to dromaeosaurs (the lineage now common- gathered that placed birds within the carnivo- ly known as ‘‘raptors’’), and that result has rous theropod dinosaurs because theropods been generally confirmed by subsequent work- apparently lacked a furcula, and Heilmann be- ers (Gauthier et al. 1988; Holtz 1994; Sereno lieved that lost features cannot re-evolve (Dol- 1997, 1999; Forster et al. 1998; Makovicky and lo’s law). Instead, Heilmann (1926) concluded Sues 1998; Zhou et al. 2000). The last 25 years that birds had evolved from ‘‘thecodonts’’—a have revealed many paleontological discover- polyphyletic garbage bag assemblage of early ies that have greatly expanded our knowledge archosaurs. It is a tribute to the careful detail of and understanding of the diversity of theropod Heilmann’s treatise that his hypothesis was so dinosaurs and Early Cretaceous birds. The re- influential given his own ambivalence about his sult has been a steady increase in support for conclusions. Heilmann described his thecodont theropod origin of birds, despite arguments to hypothesis as ‘‘wholly without shortcomings’’ the contrary (e.g. Martin 1983a, b, 1985; Fed- (i.e. character conflict) while essentially admit- uccia 1985, 1999a, b; Ruben et al. 1997; Feduccia ting that there was no evidence other than avi- and Martin 1998; Dodson 2000; Martin and an membership in the archosaurs to support it. Czerkas 2000; Jones et al. 2001). However, with Heilmann’s hypothesis became unquestioned few exceptions (e.g. Whetstone and Martin orthodoxy and was the basis of many scenarios 1981; Martin 1983a, b), critics have not proposed any explicit alternative hypothesis more detailed than Heilmann’s (1926) original vague 1 E-mail: [email protected] thecodont notion. 1 2 Perspectives in Ornithology [Auk, Vol. 119

The debate on bird origins has frequently hopes of generating a renewed interested and been portrayed by critics of the theropod hy- attention to this question within the ornithol- pothesis as a battle between ‘‘paleontologists’’ ogy community. and ‘‘ornithologists’’ (Feduccia 1999b). How- ever, this analogy has been allowed to persist EVIDENCE FOR THE THEROPOD ORIGIN for decades because of the lack of ornithologi- OF BIRDS cal participation in the debate rather than any general concordance of ornithological opinion. Evidence in support of the theropod origin of The lack of ornithological participation in this birds comes from all available sources of pale- debate can be well documented: a computer ontological evidence—largely osteology, infer- search of the recent volumes of North Ameri- ences about physiology and behavior, and can ornithological journals yields no research more recently a variety of fossilized feathers. papers including the word dinosaur in the text. Since Gauthier (1986) produced the first phy- As far as I know, Zhou’s (1995) paper on Mon- logenetic analysis of the origin of birds, sup- onychus is the only article to appear in a major port of the theropod origin of birds has been ornithological journal that deals even tangen- repeatedly upheld in phylogenetic analyses tially with the issue of avian origins since Mar- (e.g. Benton and Clark 1988; Gauthier et al. tin et al. (1980). 1988; Holtz 1994; Sereno 1997, 1999; Forster et Why is there so little ornithological interest al. 1998; Makovicky and Sues 1998). All anal- and involvement in the question of bird ori- yses have supported the same position for gins? With covers and articles in Science, Nature, birds, within a group of higher coelurosaurian Scientific American, Audubon, and National Geo- theropods which are called maniraptorans—a graphic, it cannot be because ornithologists are group that includes dromaeosaurs, or raptors not aware of it. There are two primary reasons. (e.g. Deinonychus, Velociraptor) and troodontids First, most ornithologists have not become fa- (e.g. Troodon) (Fig. 1). There have been and con- miliar enough with the primary literature de- tinue to be vigorous debates about the relative scribing the various characters to consider the positions of various theropod groups that pro- evidence for themselves. Further, few ornithol- vide opportunities for disagreement among re- ogists have formal paleontological training, searchers (e.g. tyrannosaurs and troodontids; and some may have relied on the criticism of a Holtz 1994; Sereno 1997, 1999; Makovicky and few to form the opinion that the evidence sup- Sues 1998), but all analyses have supported an porting the theropod hypothesis is flawed. The identical phylogenetic position for birds within second reason is that many ornithologists are the maniraptoran coelurosaur theropods. satisfied that the issue is irrelevant to their re- Osteological evidence of the theropod ances- search and teaching. Like many natural histo- try of birds—that is, derived characters shared rians over many centuries, ornithologists are by birds and some portion of theropod dino- generally convinced of the peculiar uniqueness saurs—comes from essentially all parts of the of birds, because we gain our professional iden- body. The evidence has been well reviewed tities as ‘‘ornithologists’’ from it. Focusing on (e.g. Witmer 1991; Padian and Chiappe 1997, the apparent uniqueness of birds may reinforce 1998; Sumida and Brochu 2000), but it is worth- our professional identities or self esteem, but it while to summarize here the extent and detail may not help us do the best possible ornitho- of the evidence explicitly for ornithologists. logical research and teaching. Theropod dinosaurs were primitively biped- Why should ornithologists care about the al, but there were several evolutionary trends in theropod origin of birds? Because the theropod theropod morphology as they evolved more ef- origin of birds is relevant to almost all aspects ficient bipedal locomotion (Gatesy 1990, 1991, of avian biology and should influence the way 1995; Gatesy and Middleton 1997; Farlow et al. we think about, study, and teach avian anato- 2000; Hutchinson 2000a, b; Hutchinson and Ga- my, behavior, physiology, ecology, and evolu- tesy 2000). Notably, the origins and insertions tion. Here, I present my perspective on the ev- of muscles that move the hindlimbs changed idence supporting the theropod origin of birds, radically, leaving observable traces on bones as the criticisms of the hypothesis, and the rele- they evolved. For example, in alligators and vance of the theropod origin to ornithology in early theropods, the M. caudofemoralis longus January 2002] Perspectives in Ornithology 3

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. The ornithischian and sauropod dinosaurs are the two immediate sister groups to the theropod dinosaurs. Taxa with 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 hypothesized to have evolved are labeled * and **, respectively. originates far out on the tail and inserts on the splint in dromaeosaurs and birds. In the ankle, fourth trocanter down the shaft of the femur; the ascending process of the astragalus became gradually, the origin of the muscle was dis- larger and evolved into the avian pretibial bone placed toward the base of the tail, and its in- (Gauthier 1986; Rieppel 1993; Padian and sertion on the femur was reduced. In modern Chiappe 1997, 1998). In the foot, the fifth toe birds, that primitively important archosaurian was reduced to a single metatarsal, and the first locomotory muscle is reduced to a thin slip, one toe was reduced and raised off the ground, of those numerous curious, vestigial pieces of leaving a functionally tridactyl foot. The first avian anatomy. Within theropods, the tail toe subsequently reevolved a lower position shortened, the basal portion of the tail shorted within birds with the evolution of the grasping even further, and the distal elements of hin- hallux. The avian pelvis also shows a number dlimbs elongated. The fibula became a thin of additional derived characters revealing the- 4 Perspectives in Ornithology [Auk, Vol. 119 ropod ancestry (Farlow et al. 2000, Hutchinson 2000b). In the group of theropods called Tetan- urans (coelurosaurs and carnosaurs), the pubis evolved a widened end, or pubic boot. In dromaeosaurs and birds, the pubic boot extends caudally and the pubis evolved a retroverted, or backward directed, position. Throughout theropods, the pubis evolved to become longer than the ischium. In the axial skeleton, theropods, like birds, have pneumatic cervical ver- tebrae that are likely indications of an early air sac system. Additional synapomorphies have been identified in the skull, including presence of an accessory antorbital fenestra and dorsal, caudal, and rostral tympanic recesses. The pectoral girdle and forelimb also reveal suites of hierarchically nested morphological novelties supporting the theropod origin of birds. In the pectoral girdle, fused clavicles, or a furcula, are now known in many theropods FIG. 2. Dorsal view of the left hands of (a) Dei- (contra Heilmann 1926; Chure and Madsen nonychus antirrhopus, (b) Archaeopteryx lithographica, 1996, Makovicky and Currie 1998, Norell et al. and (c) Nothura maculosa (Tinamidae), from Wagner 1998). The furcula is remarkably birdlike in and Gauthier (1999). Notice the common phalangeal some dromaeosaurs (Xu et al. 1999a, Burnham formulae and the similarities in proportions and et al. 2000). Also in dromaeosaurs and birds, shapes of the phalanges of digit 3 shared by Deinon- we see the derived elongate coracoids, sternal ychus and Archaeopteryx. DI–III, digits 1–3; C1–3, dis- plates (in some), and an increasingly laterally tal carpals comprising the semilunate carpal; R, ra- facing glenoid, or shoulder socket. Within the diale. (Reprinted with permission.) theropods lineage leading to birds, the forelimbs lengthened in proportion to the hind- gers. The outer two digits, number four and limbs, and the hand elongated in relation to the five, are reduced but present in Herrerasaurus rest of the forelimb. Also, some dromaeosaurs (variously hypothesized to be a basal dinosaur, and birds even show a prominently bowed ulna basal Saurischian dinosaur, or basal theropod). (e.g. Burnham et al. 2000)—a feature that Subsequently, in theropods the outer digits of zooarcheologists still use to identify avian ul- the hand are completely lost, leaving digits 1, nae in human middens. 2, and 3, as in birds. The fingers of dromaeo- The wrist of higher coelurosaurs is charac- saurs and Archaeopteryx also have the same terized by the fused distal carpals 1 and 2 (Gau- phalangeal formula (number of phalanges in thier 1986; Padian and Chiappe 1997, 1998). In each digit); the first, second, and third digits Archaeopteryx, dromaeosaurs, and even ovirap- have two, three, and four phalanges, torans and troodontids, those fused distal car- respectively. pals form a crescent-shaped bone generally Theropods also share some remarkable, de- called the semilunate carpal (Ostrom 1974; rived phalangeal proportion and shapes with Gauthier 1986; Gauthier et al. 1988; Padian and Archaeopteryx (Wagner and Gauthier 1999, Hop- Chiappe 1997, 1998). It is universally agreed son 2001). The second digit is longest in thero- that the function of that exceptional structure is pods and birds despite its fewer phalanges. In a to allow the wrists to swivel sideways. That few well-known dromaeosaurs (e.g. Deinony- feature was the character that first led Ostrom chus, Bambiraptor,andSinornithosaurus)andin (1974) to question 50 years of orthodoxy and ar- Archaeopteryx, the middle two phalanges in digit gue for the theropod origin of birds. 3 are substantially shorter than either the first or Theropods exhibit a simultaneous trend to- fourth (Fig. 2). Further, those shorter, middle ward loss of digits and the evolution of a grasp- phalanges are twisted along their axes, so that ing hand. Primitively, dinosaurs have five fin- the third digit does not flex parallel to the oth- January 2002] Perspectives in Ornithology 5 ers, but twists inward toward the center of the guments about functional and physiological hand (Wagner and Gauthier 1999, Hopson 2001). plausibility. Although critiques have been ef- That unique and bizarre morphology gives rise fectively countered in the literature many times to the curious curled position of digit 3 in many (e.g. Witmer 1991; Padian and Chiappe 1997, Archaeopteryx specimens and related dromaeo- 1998; Sumida and Brochu 2000), criticisms have saurs (e.g. Sinornithosaurus; Xu et al. 1999a). remained largely unchanged (e.g. Feduccia These new observations demonstrate that Heil- 1999a, b; Dodson 2000). mann’s (1926) reconstruction of the hand of Ar- Criticisms of phylogenetic methods. Since Gau- chaeopteryx with digit 3 lying nicely parallel to thier (1986), the bird-origin debate has really digit 2 is incorrect. Digit 3 of Archaeopteryx been about methods of analysis. Two alterna- moved independently of digit 2, maintaining a tives are represented: phylogenetic systematics, grasping function underneath the wing feathers in which explicit historical hypotheses of rela- as many specimens of Archaeopteryx show. A re- tionships among monophyletic groups are pro- vised reconstruction of the hand of Archaeopter- posed based on hypothesized shared derived yx (Fig. 2) also explains the apparently anoma- characters; and traditional eclectic narrative lous insertion of the remiges on digit 2 (the methods, that have remained essentially un- middle digit) instead of digit 3, which would be changed since Heilmann (1926), in which no the trailing edge of the wing. explicit analytical method is used, and no at- In summary, osteological synapomorphies of tempts are made to actually document the phy- birds and theropod dinosaurs come from the logenetic history of lineages related to birds. detailed similarities of many parts of the Now, phylogenetics is universally recognized body—head to toe, tip to tail. As the recent de- in systematics and evolutionary biology, and bate over the phylogenetic position of Monon- even by U.S. courts (e.g. in cases of criminal ychus (Zhou 1995, Chiappe et al. 1996, Sereno HIV infection; Vogel 1997). But, critics of the 1999) and Caudipteryx (Ji et al. 1998, Feduccia theropod origin of birds have been a singular 1999b, Jones et al. 2000a, Zhou 2000, Zhou and exception to that nearly universal intellectual Wang 2000, Zhou et al. 2000) makes clear, it is trend. Steadfastly they have maintained that increasingly difficult even to distinguish a bird phylogenetics cannot be relied upon to solve from other theropods. This summary has al- the question of the origin of birds (e.g. Feduccia most excluded consideration of the newest, 1999b, Dodson 2000). most exciting, and perhaps most compelling A few explicit alternative phylogenetic hy- fossils finds from the Yixian formation of potheses to the theropod theory have been Liaoning, China. The explosion of critical spec- proposed in recent decades—that birds are re- imens from those deposits in the last few years lated to crocodilians (Walker 1972; Whetstone has revolutionized the quality and quantity of and Martin 1981; Martin 1983a, b), or that birds evidence bearing on the origin and early evo- are related to the early archosaur Euparkeria lution of birds (Stokstad 2001). Those speci- (Welman 1995). The crocodile hypothesis has mens include conclusive evidence of the stron- been abandoned in recent years after scrutiny gest possible bird–theropod synapomorphy— of the details, and several phylogenetic analy- completely modern feathers (see below)—and ses have failed to support Euparkeria as a close the oldest, most birdlike dromaeosaurs. avian relative (Sumida and Brochu 2000). Sev- eral early archosaurs or archosaurimorphs have CRITICISMS OF THE THEROPOD ORIGIN OF BIRDS also been proposed as candidate ‘‘thecodont relatives’’ of birds (e.g. Longisquama, Scleromo- Despite the wealth of and increasing chlus,andMegalancosaurus), but not in the strict strength of the evidence, the theropod hypoth- phylogenetic sense of exclusive, shared ances- esis of the origin of birds has received unre- try. Rather, it is usually stated that birds may lenting criticism for more than two decades. have evolved through a similar morphological These criticisms can be grouped in several clas- ‘‘stage’’ (e.g. Jones et al. 2001). Because those ses: general critiques of phylogenetic methods, proposals are lacking in supporting details, criticisms of the validity and homology of spe- they do not constitute credible alternative sister cific characters, temporal disparity between the taxa. All detailed analyses of the array of alter- avian and theropod radiations, and a priori ar- native archosaurian sister-groups of birds have 6 Perspectives in Ornithology [Auk, Vol. 119 demonstrated than none has any substantial Ironically, rejection of nearly any aspect of support (Sumida and Brochu 2000). The most avian anatomy as phylogenetically informative recent proposal of feathers in the Triassic Lon- will undermine any future attempts to support gisquama (Jones et al. 2000b) received immedi- an alternative hypothesis. Thus, if the furcula ate criticisms on numerous grounds (Reisz and shared by many higher theropods and birds Sues 2000, Prum 2001, Unwin and Benton 2001, can be ignored as uninformative, how can one Prum and Brush 2002). As Sumida and Brochu argue that the presence of furcula in Megalan- (2000) point out, no alternative has any more cosaurus or Longisquama is somehow a valid than a few superficially birdlike features; but character? Critics of the theropod hypothesis phylogenetic analyses have already identified a are predictably unconcerned about that prob- group with numerous hierarchically distribut- lem because they do not actually intend to es- ed, derived morphological features shared tablish a sister group to birds. with birds—theropod dinosaurs. In a few cases, valid criticisms of the character Criticisms of the characters. A frequent criti- data have been made, but, tellingly, those criticism of the evidence in support of the theropod cisms have actually strengthened the support origin of birds has been ‘‘garbage in, garbage for the theropod hypothesis. For example, Os- out.’’ The implication is that derived character trom (1974) originally homologized the semilu- states hypothesized to be shared by birds and nate carpal with the avian radiale, but Martin theropods are too dissimilar, incorrectly ho- (1983a, b) pointed out that homology could not mologized, or functionally important and be correct because the semilunate carpal of Ar- therefore too convergent to be historically in- chaeopteryx becomes fused within the carpome- formative (e.g. see Martin et al. 1980, Martin tacarpus in higher birds, and that the radiale is and Stewart 1985, Feduccia 1999b). a proximal carpal(s). Following Martin’s obser- Characters are often rejected on the basis of vation that the semilunate carpal was composed some preconceived notion about the evolution- of distal carpals, Padian and Chiappe (1997, ary process (Padian 2001). For example, it is hy- 1998) recognized that the fusion of distal carpals pothesized that birds must have evolved flight 1 and 2 actually evolved much earlier in thero- from trees, so their ancestors must have been pods than previously recognized by Ostrom arboreal. Thus, bipedality of terrestrial thero- (1974). Subsequently, the semilunate shape of pods and birds must be convergent, and all that novel element was derived in the common hindlimb, pelvis, and tail characters can be dis- ancestor of maniraptorans. A reanalysis based counted (Feduccia 1999b). However, in parallel on Martin’s criticism provides an expanded his- with the universal adoption of phylogenetic torical context for the explanation of both the or- methods in systematics, there has been an igin of the novel element and subsequent evo- equivalent recognition that it is essential to es- lution of its unique semilunate shape. tablish a phylogenetic pattern before (e.g. Lau- If ornithologists want to evaluate the char- der 1990, Larson and Losos 1996, Lauder and acter analysis methods of some vocal critics of Rose 1996), or independently of (e.g Padian the theropod hypothesis, a good example can 2001), the analysis of functional and macroevo- be found in the quasi-phylogenetic hypothesis lutionary process. The ability to merely con- of early bird phylogeny proposed by Larry ceive of two features as convergent is consid- Martin, Alan Feduccia, and colleagues (Hou et ered by critics to be sufficient criteria to reject al. 1996). Those authors proposed that Archae- a proposed synapomorphy completely: for ex- opteryx and Confuciusornis were the sister ample Feduccia and Martin’s (1998) critique of group to enantiornithine birds, and that Liaon- the Velociraptor wishbone. However, only a phy- ingornis and Chaoyangia are the sister group to logenetic analysis that includes all proposed all other birds, including modern birds. How- characters and taxa can resolve whether char- ever, because enantiornithines had many ad- acters are phylogenetically informative. To re- vanced flight features found in modern birds, ject a hypothesis of homology, it is necessary to that hypothesis requires the convergent evolu- show that the proposed similarities evolved tion of the keeled sternum, the strut-like cora- convergently within a phylogenetic analysis in- coid, the tarsometatarsus, the shortened tail, cluding other phylogenetically informative and the pygostyle. Curiously, the modern birds characters (Patterson 1982, Pinna 1991). appear in their published phylogeny but not in January 2002] Perspectives in Ornithology 7 the unpublished data set or analysis on which langeal formula, proportions, shape, and func- it is based (Hou et al. 1996; supplemental mation shared by fingers of birds and theropods terials can be found online, see Acknowledge- must be convergent. That conclusion ‘‘is based ments). The authors decided that the tarsome- upon classical homology and reliance on the tarsi in various birds were different enough to principles of developmental position and con- conclude that all of those characters are conver- nections’’ (Feduccia 1999b:385). Of course, such gent within birds. Needless to say, most orni- reasoning only further raises the question of thologists would have difficulty in accepting how the digits of theropod hands could have that all those features had evolved convergently developed in the absence of the essential fourth in birds. Numerous phylogenetic analyses (e.g. metacarpal developmental axis, but the extinc- Chiappe 1995, Chiappe et al. 1999) have shown tion of nonavian theropods has conveniently that enantiornithines are phylogenetically closer prevented anyone from acquiring those data. to extant birds than are Archaeopteryx or Confu- Wagner and Gauthier (1999) proposed the ciusornis, supporting a single origin of those ad- ‘‘frame-shift’’ hypothesis as a solution to this vanced flight features and rejecting Hou et al.‘s apparent conflict. Essentially, they hypothesized (1996) and Martin’s (1983b) hypothesis of tar- that the theropod hand evolved to develop digits sometatarsus evolution. However, Hou et al. 1–2–3 in positions 2–3–4. Comparing the frame- (1996) demonstrates the advantages of present- shift hypothesis to Lysenkoism, cold fusion, and ing an explicit hypothesis, and documents an or- a ‘‘cladistic jihad,’’ Feduccia (1999a) suggested nithological example of the type of character that Wagner and Gauthier (1999) were denying analysis promoted by critics of the theropod hy- the developmental facts to maintain the credi- pothesis. It can be hoped that these and other bility of the theropod hypothesis. Recently, critics of the theropod hypothesis will soon at- however, Dahn and Fallon (2000) published a se- tempt a phylogenetic analysis of the nonthero- ries of experiments on development of chick hin- pod origin of birds that can be scrutinized as dlimb digits that demonstrate that amniote digit easily. identity is not an inherent property of the digit 1–2–3 versus 2–3–4. One criticism of the the- primordia or their positions. Rather, identity of ropod hypothesis deserves detailed consider- the developing digit primordia is initially un- ation because it has frequently been cited as the specified despite their positions. Instead, digit biggest obstacle to the theropod origin of birds. identity is determined by the interactions be- The avian hand has three digits. On the basis tween the digit primordia and gradients of pat- of phylogenetic analyses of digit reduction in dinosaurs, theropods are universally recog- tern formation genes (e.g. bone morphogenetic nized as having digits 1–2–3 (Hinchliffe 1985; proteins, or ‘‘BMPs’’) in the interdigital meso- Wellnhofer 1985; Burke and Feduccia 1997; Pa- derm that surrounds the digit primordia early in dian and Chiappe 1997, 1998; Feduccia 1999a, development (Dahn and Fallon 2000). By trans- b; Wagner and Gauthier 1999). In contrast, de- planting digit primordia and the interdigital velopmental biologists have traditionally re- mesoderm within and among chick feet, they ex- ferred to the digits of the hand in birds as 2–3– perimentally created homeotic transformations 4 (Hinchliffe 1985; Burke and Feduccia 1997; (i.e. changes to the identity of any digit) and Feduccia 1999a, b; Wagner and Gauthier 1999), grew any digit in any position (Fig. 3). Further, because the first cartilage condensation to de- by experimentally manipulating BMP levels in velop in the hand (and foot) of most amniotes the interdigital mesoderm, Dahn and Fallon becomes distal carpal 4 and metacarpal 4, and (2000) could anteriorize or posteriorize all digits the most posterior digit in the avian hand ul- of the hand (as hypothesized by the frame-shift timately develops above this first condensation hypothesis; Fig. 3). They were even able to pre- (Hinchliffe 1985, Burke and Feduccia 1997). dictably grow digits with extreme phalangeal Thus, the traditional developmental hypothesis formulae that do not occur among known ar- is that the digit that develops above metacarpal chosaurs. Interestingly, as developmental biolo- 4 is digit 4 because its identity is determined by gists, R. D. Dahn and J. F. Fallon (pers. comm.) its position. Therefore, fingers of birds must be were entirely uninvolved with the paleontolog- digits 2–3–4, they cannot be homologous with ical and systematic debate on the homology of those of theropods, and all similarities in pha- digits of the avian hand. 8 Perspectives in Ornithology [Auk, Vol. 119

FIG. 3. Control and experimental homeotic transformations of digit identity in the foot of chicks (Gallus gallus) from Dahn and Fallon (2000). (A) The standard phalangeal formula with digits1–4 having 2–5 phalanges, respectively. (B) Homeotic transformation of of all digit identities produced by beads (dots) with Sonic Hedgehog protein between digits. Each digit has an additional phalanx, typical of posteriorization of digit 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 of a phalanx, or an anteriorization of digit identity. (Reprinted with permission.)

Dahn and Fallon’s (2000) work provides mo- raptoran, and other theropod fossils included lecular developmental evidence supporting the in the hypothesis are best known from the Late plausibility of the frame-shift hypothesis (Galis Cretaceous, or about 80 Ma, but many are 2001). It is entirely plausible for theropods to known from much earlier. The notion of a tem- have evolved changes in patterns of BMP ex- poral paradox is based on several fundamental pression in the developing hand that would misconceptions about paleontology and evo- lead to a frame-shift in digit identity. Further- lutionary biology (Padian and Chiappe 1998), more, Dahn and Fallon’s (2000) data falsify the and by misrepresentation of the evidence (Pa- primary assumption of 2–3–4 hypothesis: that dian and Chiappe 1998, Brochu and Norell the conserved patterns of metacarpal develop- 2000). ment within the hand dictate digit identity. Far The first misconception is thinking purely in from ‘‘accommodating the cladogram’’ (Fed- terms of prephylogenetic ancestor–descendant uccia 1999a), Wagner and Gauthier (1999) made relationships. For example, A. Feduccia has of- a bold prediction that the developmental un- ten repeated that birds cannot be related to the- derstanding of digit identity must be incom- ropod dinosaurs because ‘‘you can’t be your plete. Dahn and Fallon (2000) independently own grandmother.’’ However, phylogenetic hy- demonstrated that this prediction was correct. potheses are statements about the history of Although many details remain to be investi- shared ancestry among lineages. The theropod gated, it is now clear that there is no conflict be- hypothesis does not imply that Deinonychus,or tween the theropod hypothesis of bird origins any other Late Cretaceous dromaeosaur, is ac- and the facts of developmental biology. tually ancestral to birds. Rather, the theropod ‘‘Temporal paradox’’. Another criticism of the hypothesis proposes that those organisms theropod hypothesis is the supposed ‘‘tempo- shared an exclusive common ancestor. Further, ral paradox’’—the notion that theropod diver- Feduccia (1999b:90) has stated that ‘‘one could sity is too young to be phylogenetically closely interpret the temporal evidence as indicating related to birds. The objection has been that that birds and dinosaurs are indeed examples fossils presumed to be closest to birds are too of convergent evolution.’’ Such reasoning im- late in time compared to the first bird, Archae- plies that distribution of stochastic samples in opteryx, approximately 148 my old (Sereno paleontological time can be used to reject a 1997). Many dromaeosaurs, ornithomimid, ovi- phylogenetic analysis based on many detailed January 2002] Perspectives in Ornithology 9 characters that are directly observable. Lastly, transitions are evolutionarily likely or impos- critics imply that such temporal disjunctions sible, and then use that ‘‘knowledge’’ of how are rare or unexpected. But, as Padian and evolution works to reject phylogenetic analyses Chiappe (1998) point out, the fossil record of based on a wealth of character evidence. Ex- monotremes goes back less than 20 Ma, where- amples include numerous analyses of the ori- as the fossil record of therian mammals goes gin of avian flight (e.g. Feduccia 1985, Tarsitano back 100 Ma. Yet, no one could credibly argue 1985), lung ventilation (Ruben et al. 1997), and that this 80 my temporal disjunction could af- homeothermy and growth rates (Ruben and fect our confidence that monotremes are the sis- Jones 2000). These particular issues have been ter group to all other extant mammals. rebutted well elsewhere (Padian and Chiappe The magnitude of the supposed temporal 1998, Padian et al. 2001, Perry 2001). paradox has also been greatly and repeatedly exaggerated. Recently, Feduccia and Martin IMPLICATIONS OF THE THEROPOD ORIGIN (1998), Feduccia (1999b), and Dodson (2000) all OF BIRDS characterized the temporal disjunction between Archaeopteryx and dromaeosaurs as be- Is the theropod origin of birds relevant to the tween 60–80 my. Those authors have plainly ig- biology of modern birds? Advances in applying nored fragmentary fossils indicating existence phylogenetic methods to many questions in of dromaeosaurs in the Late Jurassic (Jenson ecology and behavior have helped demonstrate and Padian 1989). Furthermore, at least three the relevance of phylogenetic history of many taxa of basal dromaeosaurs are now known aspects of avian biology, but many ornitholo- from the 124 Ma old Yixian formation of Liaon- gists may think that those ancient events are ing, China (Xu et al. 1999b, 2000, 2001; Ji et al. not important. Actually, I think that the impli- 2001) which is only 24 my younger than Ar- cations of the theropod origin of birds to the bi- chaeopteryx. Not only are these new taxa the ology of modern birds are many, broad, and oldest, well-known dromaeosaurs, but they are varied, and that the theropod origin should be the most birdlike theropods in many features, fundamental to how we think about and study including their small size and obvious feathers. avian biology. Here, I will review a series of If a temporal paradox ever existed, it has been examples. substantially reduced to between 0 and 24 my. Feathers. Possesion of feathers has been con- Stated phylogenetically, the temporal para- sidered as synonymous with birds by human dox assumes that sister taxa should have the cultures essentially forever (with exceptions for same data of origin in the fossil record. That ex- angels; Pinna 1991). Recent paleontological pectation is unrealistic given the inherent discoveries have demonstrated that feathers patchiness of the paleontological record. For originated and diversified in theropod dino- example, the handful of specimens of Archae- saurs before the origin of birds and of flight opteryx are themselves amazing chronological (Chen et al. 1998; Ji et al. 1998, 2001; Schweitzer outliers given the lack of any other known Ju- et al. 1999; Sereno 1999; Xu et al. 1999a, b, 2000, rassic birds. Until very recent discoveries from 2001; Padian 2001; Sues 2001; Prum and Brush the Early Cretaceous in China (Stokstad 2001), 2002). I discuss this topic here because I want even very few Early Cretaceous birds were to emphasize the implication of these data for known (Martin 1983a). Of course, the temporal how we think about and how we need to re- disjunction between Archaeopteryx and other think avian biology (see Prum and Brush 2002 birds does not lead us to question the mono- for thorough review). phyly of birds. Furthermore, Brochu and Norell In the last five years, the Early Cretaceous (2000) have demonstrated that the ‘‘temporal Yixian formation of China and the Late Creta- paradox’’ is equivalent or even greater for all ceous of Mongolia have produced fossils of proposed alternatives to the theropod hypoth- eight nonavian theropod dinosaurs that have esis of avian origins. filamentous integumental appendages that Functional and physiological criticisms. An- have been hypothesized to be homologous with other common method used to criticize the the- avian feathers: Sinosauropteryx (Chen et al. ropod hypothesis is to make a priori assump- 1998), Shuvuuia (Schweitzer et al. 1999), Bei- tions about which functional or physiological piaosaurus (Xu et al. 1999b), Caudipteryx (Ji et al. 10 Perspectives in Ornithology [Auk, Vol. 119

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

1998), Protarchaeopteryx (Ji et al. 1998), Sinor- ed that they share three unique features with nithosaurus (Xu et al. 1999a, 2001), Microraptor avian feathers: multiple filament structure, bas- (Xu et al. 2000), and an unnamed basal dro- al branching, and serial branching (Fig. 4; Xu et maeosaur (Ji et al. 2001). One of those taxa, al. 2001). Subsequently, the integumentary ap- Caudipteryx, has indisputable evidence of pendages of an unnamed but closely related branched, pennaceous feathers (Ji et al. 1998), dromaeosaur taxon further document a vane of and repeated phylogenetic analyses based on parallel barbs running at an acute angle in ex- numerous characters have demonstrated that actly the conformation of a pennaceous feather Caudipteryx is a basal oviraptoran dinosaur (Ji et al. 2001). Those fossil structures are es- (Sereno 1999, Zhou 2000, Zhou and Wang 2000, sentially indistinguishable from the contour Zhou et al. 2000). Critics of the theropod hy- feathers of confuciusornithine and enantiorni- pothesis have called that taxon a secondarily thine birds preserved in the same strata. flightless bird based only on its body propor- New theropod integumental structures have tions (Jones et al. 2000a), or brief discussion of been repeatedly dismissed as connective tis- a few characters in absence of any explicit anal- sues, such as frayed collagen fibers or ossified ysis of the character data (e.g. Martin and Czer- tendons (Feduccia 1999a, b; Martin and Czer- kas 2000). Sinosauropteryx is a basal coelurosaur kas 2000; Ruben and Jones 2000). But none of with small (about 5–6 mm) integumentary ap- those critics have explained why a therizino- pendages that are apparently cylindrical, and saur would have 70 mm collagen filaments may also be branched in some fashion (Chen et hanging of the trailing edge of its ulna in the al. 1998). Beipiaosaurus (a therizinosaur), and exact position of avian remiges (Xu et al. Sinornithosaurus, Microraptor, and another un- 1999b); why a dromaeosaur (Sinornithosaurus) named taxon (all basal dromaeosaurs) all have would have a 35 mm ossified tendon emerging long filamentous integumentary appendages from the tip of its snout (Xu et al. 2001); or why that are diverse in size and structure (Xu et al. collagen fibers would be indistinguishable 1999a, b, 2000, 2001; Ji et al. 2001). Detailed from feathers preserved in the same rock? Fur- analyses of the structure of integumentary ap- ther, there is now paleobiochemical evidence pendages of Sinornithosaurus have demonstrat- that the filamentous integumentary append- January 2002] Perspectives in Ornithology 11 ages of Shuvuuia, an alvarezsaurid related to wing ‘‘gait’’ (i.e. a continous wing vortex), and the ornithomimid theropods, are composed of fewer morphological specializations than does ␤-keratin (Schweitzer et al. 1999) which occurs flying at slower speeds or taking off from the only in the epidermis. ground (which require a ring-vortex). This fact The theropod origin of feathers (Padian 2001, places a substantial functional challenge to Sues 2001, Prum and Brush 2002) has tremen- how a terrestrial biped could have evolved dous implications for avian biology. Possession flight purely from the ground. However, Bur- of feathers is no longer synonymous with birds, gers and Chiappe (1999) recently pointed out nor did feathers evolve for flight. Feathers orig- that previous models had ignored the fact that inated and diversified in terrestrial theropod flapping feathered wings while running will dinosaurs, and were only subsequently co-opted considerably increase the ground speed before to function in flight by birds (Prum and Brush take off. Consequently, they hypothesize Ar- 2002). Feathers can no longer be considered the chaeopteryx and the maniraptoran ancestors of reason why birds survived the Cretaceous–Ter- all birds could have become airborne by flap- tiary boundary, because numerous lineages of ping and running simultaneously. We may feathered theropods went extinct at this time. never have definitive evidence of the ecological Why did birds survive? That question can be context—arboreal or terrestrial—of the origin addressed in future research without feathers of flight in theropods, but it is clear from cur- as a consideration. rent evidence that the major components of the Flight. The theropod origin of birds and flight stroke had already evolved in bipedal feathers has important implications for the evo- theropods in a wholly terrestrial context (Gau- lution of avian flight. The origin of birds, feath- thier and Padian 1985; Padian and Chiappe ers, and avian flight are the central trinity of ear- 1997, 1998). ly avian evolution. Unfortunately, these three Terrestrial locomotion. The theropod origin questions are frequently addressed as interde- of birds also has other important implications pendent and correlated hypotheses. Critics of for the evolution of avian terrestrial locomo- the theropod hypotheses usually advocate a the- tion. Gatesy and Dial (1996) observed that the codont origin of birds, an aerodynamic origin of evolution of avian flight required decoupling of feathers, and an arboreal origin of flight (Fed- the coordinated forelimb and hindlimb move- uccia 1999b). In contrast, supporters of the the- ments that are a primitive feature of reptilian ropod hypothesis have usually advocated a locomotion, and the evolution of a novel neu- thermoregulatory origin of feathers and a ter- rological motor coupling of forelimb and tail restrial origin of flight (Ostrom 1974). Unfortu- movements. Because bipedal locomotion was nately, treating those hypotheses as necessarily primitive to theropods, forelimbs and hin- interdependent is scientifically constraining, un- dlimb movements had already been evolution- productive, and unnecessary. There is nothing arily decoupled within that lineage. Thus, as about the theropod origin of birds that excludes flight evolved in birds, new neuromuscular as- the possibility that flight could have evolved sociations could evolve between wing and tail from tress (e.g. Chatterjee 1997). However, the function required for controlled flight without theropod origin of birds makes it clear that an- compromising terrestrial locomotion. Gatesy cestors of birds were cursorial bipeds, and that and Dial’s (1996) observations of avian loco- many of the morphological features that were motor modules underscores another challenge ultimately co-opted, or exapted (Gould and to the traditional arboreal theory of the origin Vrba 1982), in the evolution of the wing and the of flight, which proposes that avian flight flight stroke evolved in a terrestrial context for a evolved directly from lizardlike quadrapedal purpose other than flight (Gauthier and Padian arboreal ancestors. 1985; Padian and Chiappe 1997, 1998; Padian Steve Gatesy and colleagues (Gatesy 1990, 2001). Those characters include numerous fea- 1991, 1995; Gatesy and Dial 1996; Gatesy and tures of the forelimb, shoulder girdle, wrist, and Middleton 1997; Hutchinson and Gatesy 2000) manus that allowed birds to evolve a flight have done a number of comparative analyses of stroke from a prey grasping movement. the evolution of terrestrial locomotion in birds Rayner (1985) and others have pointed out and other theropods. This body of work has un- that flying at faster speeds requires a simpler derscored the functional continuity between 12 Perspectives in Ornithology [Auk, Vol. 119 birds and other theropods, while also identi- ing individual are held at the sides but distinct- fying derived features of avian locomotion and ly apart from the body as if covering the rest of placing them in an historical context. For ex- the clutch with its wing feathers. Thus, another ample, John Hutchinson (2000a, b) has done eminently avian feature—brooding—likely comparative phylogenetic analyses of the evo- also had an origin somewhere in theropod di- lution of the shapes of the theropod and avian nosaurs prior to the evolution of birds. pelvis and femur; the origins, insertions, and David Varricchio and colleagues (Varricchio sizes of various hindlimb muscles; and the lo- et al. 1999) have been conducting research on comotor consequences of those changes (Fig. the nest of Troodon formosus that reveal some 4). He concludes that many muscular features more remarkably birdlike details to theropod thought to be unique to birds can be under- reproduction. Troodon and other theropods stood historically as the extreme in a continu- probably laid pairs of eggs, instead of single um of morphological character state evolution. eggs as in most birds, because they still had Morphologically and functionally, extant birds two ovaries. The 24 eggs in each clutch were are much less distinct, and therefore more eas- laid in pairs instead of all at once, which is the ily understood, in the context of their theropod primitive condition of crocodylians and most origin. This groundbreaking body of work by other reptiles. Thus, the clutch appears to be Gatesy, Hutchinson, and colleagues demon- composed over a series of days, and another strates vividly how the theropod hypothesis of distinct feature of avian reproduction appears avian origins provides an historical context for to have originated in the theropod ancestors of understanding extant avian diversity. birds. The typical avian traits of having one Nesting biology and clutch size. Perhaps few functional ovary and laying single eggs per day features of avian biology have been as well are apparently derived in birds. So, serial com- studied as reproductive behavior and ecology. position of the clutch was not a weight-reduc- Yet it is little appreciated that fundamental as- tion adaptation for flight because it apparently pects of avian reproductive biology evolved evolved in theropods before the origin of flight. during early archosaurian and theropod ances- Another interesting feature of the Troodon try. For example, birds are often considered nests is their clutch size. One of the fundamen- unique among vertebrates for the extent and tal limitations on the size of a clutch laid over ubiquity of parental care. It is easy to see, how- a series of days is the time it takes for an un- ever, that extensive parental care is primitive to incubated egg to spoil. If a clutch takes too archosaurs. Crocodylians have obligatory nest many days to complete, then the first eggs laid building, nest defense, and extensive post- will begin to spoil before the entire clutch is in- hatching parental care. Young pterosaurs were cubated. Like birds, Troodon likely delayed incapable of flight during early growth, and brooding until the entire clutch was complete must have received extensive parental care in to synchronize hatching. Although the Troodon early life (Ricqle`s et al. 2000). The evidence of clutch size was 24, it was likely laid over ϳ12 nesting and parental care in ornithischian, sau- days, corresponding to an avian clutch size of ropod, and theropod dinosaurs is extensive 12 eggs. So, it is possible that one of the pri- (Currie and Padian 1997). Thus, this funda- mary determinants of clutch size in precocial mental feature of avian biology is not exclu- birds has persisted since the origin of serial sively avian, but essentially archosaurian. clutch assembly in the theropod ancestors of The most dramatic evidence of similarity of birds. paternal care in birds and other theropods Growth and metabolic rates. Avian growth comes from the nests of Oviraptor found in and metabolic rates are of great interests to Mongolia (Clark et al. 1999). This striking fossil ecologists and physiologists. Recently, Padian shows an Oviraptor (erroneously believed to be et al. (2001) reviewed the evidence of dinosaur stealing eggs when first described!) lying on growth rates and metabolic rates inferred from top of a terrestrial clutch of eggs in a perfectly paleohistology. A conservative conclusion is fossilized brooding posture. Unlike the primi- that dinosaurs evolved substantially higher tive archosaurian condition found in croco- growth rates than other archosaurs and rep- diles, Oviraptor did not place vegetation over tiles, further substantiating the hypothesis that the top of the nest. The forelimbs of the brood- dinosaurs were not typical ectotherms. The January 2002] Perspectives in Ornithology 13 evolution of growth rates in early birds is also can ornithologists participate? First, the the- interestingly complex. Some lineages appear to ropod origin of birds and general dinosaur bi- show conspicuously slower growth rates than ology should be taught in all introductory or- were typical of their theropod ancestors (e.g. nithology courses. The Encyclopedia of Dinosaurs confuciusornithine and enantiornithine birds). (Currie and Padian 1997) is an excellent place Padian et al. (2001) hypothesize that this may to start for supplemental material. (Interested have been associated with the initial evolution ornithologists can also contact the author for of small size in early birds. Subsequently, sample lecture notes.) Basic dinosaur biology growth rates increased again in modern birds. and the theropod origin of birds should be in- As with many other features of avian biology, corporated in all future ornithology textbooks: investigation of the theropod context of avian there is not a single chapter of a standard or- origins establishes that many characteristics nithological text that could not include addi- previously thought to be unique to birds can be tional insights on avian biology based on their understood to have evolved in their more an- theropod origin. But textbooks are based on the cient avian ancestors. scientific literature. It will be important for ornithologists to become broadly familiar with dinosaur diversity and apply their knowledge CONCLUSIONS of birds to the larger field of dinosaur and ar- The theropod hypothesis of the origin of chosaur biology. Ornithologists should develop birds is the only phylogenetically explicit hy- research partnerships with dinosaur paleon- pothesis available for the relationships of birds tologists, and paleontological papers on non- to other archosaurs. Shared derived anatomical avian dinosaur biology with implications for characters in support of this hypothesis come ornithology should be published in ornitholog- from all parts of the skeleton, and recent fossil ical journals. There are now many examples of evidence also documents that fully modern, research that bridges the narrowing gap be- pennaceous feathers, and many birdlike repro- tween birds and other dinosaurs and genuinely ductive behaviors evolved in theropod dino- contribute to ornithological knowledge (e.g. Gatesy and Middleton 1997; Wagner and Gau- saurs before the origin of birds. The theropod thier 1999; Hutchinson 2000a, b). origin of birds has important implications for Until any credible alternative is proposed, it research and teaching in all fields of ornithol- is time to abandon debate on the theropod or- ogy. The theropod hypothesis of the origin of igin of birds, and to proceed to investigate all birds has already generated startling new pre- aspects of the biology of birds in light of their dictions about other fields of biology that have theropod origin. This fertile frontier of knowl- been confirmed by independent research—for edge promises to be among the most exciting example the development of digit identity in developments in ornithology in the coming amniotes. The theropod hypothesis implies century, and ornithologists should be actively that numerous archetypical avian features interested in and participating in this field. The evolved in theropod dinosaurs before the ori- time has come for our discipline to realize that gin of birds or flight, including feathers, hollow ornithology is extant dinosaur biology. Orni- bones, the wishbone, and likely air sacs, brood- thology can only profit as a result. ing, and serial composition of the clutch. Phy- logenetic analyses of morphology further dem- Note added in proof: Norell et al. (2002) de- onstrate that the evolution of avian anatomy scribe a new specimen of a basal dromaeosaur can be coherently understood in terms of the (possibly a Sinornithosaurus) from the 124 Ma theropod ancestry of birds (e.g. Hutchinson old Yixian formation of China that has pre- 2000a, b). These discoveries have not only ex- served impressions of modern pennaceous panded our knowledge of early bird evolution feathers including a rachis, barbs, and a planar (Chiappe 1995, Padian and Chiappe 1998), but vane. Occasional separation of barbs in the they challenge ornithologists to revise our di- feather vanes document presence of differenti- agnosis of what a bird is. ated barbules as in Archaeopteryx and modern Our understanding the relevance of thero- birds. Feathers on the tip of the tail are Ͼ19 cm pod origins to ornithology is just beginning. long, and the beautifully preserved feathers on Numerous insights await future research. How the upper hindlimbs are 13.5 cm long. This lat- 14 Perspectives in Ornithology [Auk, Vol. 119 est discovery conclusively demonstrates the CHIAPPE,L.M.,M.A.NORELL, AND J. M. CLARK. theropod origin of feathers and birds. 1996. Phylogenetic position of Mononychus from the Upper Cretaceous of the Gobi Desert. Mem- oires of the Queensland Museum 39:557–582. ACKNOWLEDGMENTS CHURE,D.J.,AND J. H. MADSEN. 1996. On the pres- I would like to thank K. Padian and T. Peterson ence of furculae in some non-maniraptoran the- for helpful comments on the manuscript. I would ropods. Journal of Vertebrate Paleontology 16: also like to thank C. Brochu, A. Brush, L. M. Chiap- 573–577. pe, S. Gatesy, J. Gauthier, J. Hutchinson, K. Middle- CLARK,J.M.,M.NORELL, AND L. M. CHIAPPE. 1999. ton, M. Norell, S. Sumida, G. Wagner, X. Xu, and Z. An oviraptorid skeleton from the Late Creta- Zhou for additional inspiration in conversation and ceous of Ukhaa Tolgod, Mongolia, preserved in in print. Supplemental materials to Hou et al. 1996 an avianlike brooding posture over an ovirap- can be found online at http://www.sciencemag. torid nest. American Museum Novitates 3256:1– org/feature/data/hou.shl. 36. CURRIE,P.J.,AND K. PADIAN,ED. 1997. The Encyclo- LITERATURE CITED pedia of Dinosaurs. Academic Press, San Diego, California. BENTON,M.J.,AND J. M. CLARK. 1988. Archosaur DAHN,R.D.,AND J. F. FALLON. 2000. Interdigital reg- phylogeny and the relationships of the Crocod- ulation of digit identity and homeotic transfor- ylia. Pages 295–338 in The Phylogeny and Clas- mation by modulated BMP signaling. Science sification of Tetrapods, vol. 1: Amphibians, Rep- 289:438–441. tiles, and Birds (M. J. Benton, Ed.). Clarendon DALTON, R. 2000. Feathers fly in Beijing. Nature 405: Press, Oxford. 992. BOCK, W. J. 1965. The role of adaptive mechanisms in DODSON, P. 2000. Origin of birds: The final solution? the origin of higher levels of organization. Sys- American Zoologist 40:505–512. tematic Zoology 14:272–300. FARLOW, J. O., S. M. GATESY,T.R.HOLTZ,JR., J. R. BROCHU,C.A.,AND M. A. NORELL. 2000. Temporal HUTCHINSON, AND J. M. ROBINSON. 2000. The- congruence and the origin of birds. Journal of ropod locomotion. American Zoologist 40:640– Vertebrate Paleontology 20:197–200. 663. BURGERS,P.,AND L. M. CHIAPPE. 1999. The wing of FEDUCCIA, A. 1985. On why the dinosaurs lacked Archaeopteryx as a primary thrust generator. Na- feathers. Pages 75–79 in The Beginnings of Birds ture 399:60–62. (M. K. Hecht, J. H. Ostrom, G. Viohl, and P.Well- BURKE,A.C.,AND A. FEDUCCIA. 1997. Developmen- nhofer, Eds.). Freunde des Jura-Museum Eich- tal patterns and identification of homologies in sta¨tt, Germany. the avian hand. Science 278:666–668. FEDUCCIA, A. 1999a. 1,2,3 ϭ 2,3,4: Accommodating BURNHAM,D.A.,K.L.DERSTLER,P.J.CURRIE,R.T. the cladogram. Proceedings of the National BAKKER,Z.ZHOU, AND J. H. OSTROM. 2000. Re- Academy of Sciences USA 96:4740–4742. markable new birdlike dinosaur (Theropoda: FEDUCCIA, A. 1999b. The Origin and Evolution of Maniraptora) from the Upper Cretaceous of Birds, 2nd ed. Yale University Press, New Haven, Montana. University of Kansas Paleontological Connecticut. Contributions—New Series 12–13:1–14. FEDUCCIA,A.,AND L. D. MARTIN. 1998. Theropod- CAMPBELL,B.,AND E. LACK. 1985. A Dictionary of bird link reconsidered. Nature 391:754. Birds. T. A. and D. Poyser, London. FORSTER,C.A.,S.D.SAMPSON,L.M.CHIAPPE, AND CHATTERJEE, S. 1997. The Rise of Birds: 225 Million Years of Evolution. Johns Hopkins University D. W. KRAUSE. 1998. The theropod ancestry of Press, Baltimore, Maryland. birds: New evidence from the Late Cretaceous of CHEN, P.-J., Z. M. DONG, AND S. N. ZHEN. 1998. An Madagascar. Science 279:1915–1919. exceptionally well-preserved theropod dinosaur GALIS, F. 2001. Digit identity and digit number: In- from the Yixian formation of China. Nature 391: direct support for the descent of birds from the- 147–152. ropod dinosaurs. Trends in Ecology and Evolu- CHIAPPE, L. M. 1995. The first 85 million years of avi- tion 16:16. an evolution. Nature 378:349–355. GARDINER, B. G. 1982. Tetrapod classification. Zoo- CHIAPPE,L.M.,Q.JI,S.JI, AND M. A. NORELL. 1999. logical Journal of the Linnean Society 74:207– Anatomy and systematics of the Confuciusor- 232. nithidae (Theropoda: Aves) from the late Meso- GATESY, S. M. 1990. Caudofemoral musculature and zoic of northeastern China. Bulletin of the the evolution of theropod locomotion. Paleobi- American Museum of Natural History, no. 242. ology 16:170–186. January 2002] Perspectives in Ornithology 15

GATESY, S. M. 1991. Hind limb scaling in birds and ses in an evolutionary context. Science 276:227– other theropods: Implications for terrestrial lo- 232. comotion. Journal of Morphology 209:83–96. HUTCHINSON, J. R. 2000a. The evolution of femoral GATESY, S. M. 1995. Functional evolution of the hind osteology and soft tissues on the line to extant limb and tail from basal theropods to birds. Pag- birds (Neornithes). Zoological Journal of the es 219–234 in Functional Morphology in Verte- Linnean Society 131:169–197. brate Paleontology (J. Thomason, Ed.). Cam- HUTCHINSON, J. R. 2000b. The evolution of pelvic os- bridge University Press, Cambridge, United teology and soft tissues on the line to extant Kingdom. birds (Neornithes). Zoological Journal of the GATESY,S.M.,AND K. P.DIAL. 1996. Locomotor mod- Linnean Society 131:123–168. ules and the evolution of avian flight. Evolution HUTCHINSON,J.R.,AND S. M. GATESY. 2000. Adduc- 50:331–340. tors, abductors, and the evolution of archosaur GATESY,S.M.,AND K. M. MIDDLETON. 1997. Biped- locomotion. Paleobiology 26:734–751. alism, flight, and the evolution of locomotor di- HUXLEY, T. H. 1868. Remarks upon Archaeopteryx versity. Journal of Vertebrate Paleontology 17: lithographica. Proceedings of the Royal Society of 308–329. London 16:243–248. AUTHIER LUGE AND OWE G ,J.,A.G.K , T. R . 1988. Am- HUXLEY, T. H. 1870. Further evidence of the affinity niote phylogeny and the importance of fossils. between dinosaurian reptiles and birds. Quar- Cladistics 4:105–209. terly Journal of the Geological Society of London GAUTHIER,J.,AND K. PADIAN. 1985. Phylogenetic, 26:12–31. functional, and aerodynamic analyses of the or- JENSON,J.A.,AND K. PADIAN. 1989. Small pterosaurs igin of birds and their flight. Pages 185–197 in and dinosaurs from the Uncompahgre Fauna The Beginnings of Birds (M. K. Hecht, J. H. Os- (Brushy Basin Member, Morrison Formation, Ti- trom, G. Viohl, and P. Wellnhofer, Eds.). Freunde thonian), Late Jurassic, western Colorado. Jour- des Jura-Museum, Eichsta¨tt, Germany. nal of Paleontology 63:364–373. GAUTHIER, J. A. 1986. Saurischian monophyly and JI,Q.,P.J.CURRIE,M.A.NORELL, AND S.-A. JI. 1998. the origin of birds. Memoires of the California Two feathered dinosaurs from northeastern Chi- Academy of Sciences 8:1–55. na. Nature 393:753–761. GOULD,S.J.,AND E. S. VRBA. 1982. Exaptation—A JI, Q., M. A. NORELL, K.-Q. GAO, S.-A. JI, AND D. REN. missing term in the science of form. Paleobiolo- 2001. The distribution of integumentary struc- gy 8:4–15. tures in a feathered dinosaur. Nature 410:1084– HEILMAN, G. 1926. The Origin of Birds. H.F.G. With- 1088. erby, London. JONES,T.D.,J.O.FARLOW,J.A.RUBEN,D.M.HEN- HINCHLIFFE, J. R. 1985. ‘‘One, two, three’’ or ‘‘two, DERSON, AND W. J. H ILLENIUS. 2000a. Cursorial- three, four’’: An embryologist’s view of the ho- ity in bipedal archosaurs. Nature 406:716–718. mologies of the digits and carpus of modern JONES,T.A.,J.A.RUBEN,L.D.MARTIN,E.N.KU- birds. Pages 141–147 in The Beginnings of Birds (M. K. Hecht, J. H. Ostrom, G. Viohl, and P.Well- ROCHKIN,A.FEDUCCIA,P.F.A.MADERSON,W.J. nhofer, Eds.). Freunde des Jura-Museum, Eichs- HILLENIUS,N.R.GEIST, AND V. A LIFANOV. ta¨tt, Germany. 2000b. Non-avian feathers in a late Triassic ar- HOLTZ, T. R. 1994. The phylogenetic position of the chosaur. Science 288:2202–2205. Tyrannosauridae: Implications for theropod sys- JONES,T.D.,J.A.RUBEN,P.F.A.MADERSON, AND L. tematics. Journal of Paleontology 68:1100–1117. D. MARTIN. 2001. Longisquama fossil and feather HOPSON, J. A. 2001. Ecomorphology of avian and morphology. Science 291:1899–1902. nonavian theropod phalangeal proportions: Im- LARSON,A.,AND J. A. LOSOS. 1996. Phylogenetic sys- plications for the arboreal versus terrestrial ori- tematics of adaptation. Pages 187–220 in Adap- gin of bird flight. Pages 211–235 in New Per- tation (G. V. Lauder and M. R. Rose, Eds.). Aca- spectives on the Origin and Early Evolution of demic Press, San Diego, California. Birds (J. Gauthier and L. F. Gall, Eds.). Peabody LAUDER, G. V. 1990. Functional morphology and sys- Museum of Natural History, Yale University, tematics: Studying functional patterns in an his- New Haven, Connecticut. torical context. Annual Review of Ecology and HOU,L.,L.D.MARTIN,Z.ZHOU, AND A. FEDUCCIA. Systematics 21:317–340. 1996. Early adaptive radiation of birds: Evidence LAUDER,G.V.,AND M. R. ROSE,EDS. 1996. Adapta- from fossils from northeastern China. Science tion. Academic Press, San Diego, California. 274:666–668. MAKOVICKY,P.J.,AND P. J. C URRIE. 1998. The pres- HUELSENBECK,J.P.,AND B. RANNALA. 1997. Phylo- ence of a furcula in tyrannosaurid theropods, genetic methods come of age: Testing hypothe- and its phylogenetic and functional implica- 16 Perspectives in Ornithology [Auk, Vol. 119

tions. Journal of Vertebrate Paleontology 18:143– Eds.). Peabody Museum of Natural History, Yale 149. University, New Haven, Connecticut. MAKOVICKY,P.J.,AND H.-D. SUES. 1998. Anatomy PINNA, M. C. 1991. Concepts and tests of homology and phylogenetic relationships of the theropod in the cladistic paradigm. Cladistics 7:367–394. dinosaur Microventer celer from the Lower Cre- PRUM, R. O. 1999. Development and evolutionary or- taceous of Montana. American Museum Novi- igin of feathers. Journal of Experimental Zoolo- tates 3240:1–27. gy (Molecular and Developmental Evolution) MARTIN, L. D. 1983a. The origin and early radiation 285:291–306. of birds. Pages 291–338 in Perspectives in Orni- PRUM, R. O. 2001. Longisquama fossil and feather thology (A. H. Brush and G. A. Clark, Eds.). morphology. Science 291:1899–1900. Cambridge University Press, Cambridge, United PRUM,R.O.,AND A. H. BRUSH. 2002. The evolution- Kingdom. ary origin and diversification of feathers. Quar- MARTIN, L. D. 1983b. The origin of birds and of avian terly Review of Biology 77:in press. flight. Current Ornithology 1:106–129. RAYNER, J. M. V. 1985. Cursorial gliding in proto- MARTIN, L. D. 1985. The relationship of Archaeopteryx birds. Pages 289–302 in The Beginnings of Birds to other birds. Pages 177–183 in The Beginnings (M. K. Hecht, J. H. Ostrom, G. Viohl, and P.Well- of Birds (M. K. Hecht, J. H. Ostrom, G. Viohl, and nhofer, Eds.). Freunde des Jura-Museum, Eichs- P. Wellnhofer, Eds.). Freunde des Jura-Museum, ta¨tt, Germany. Eichsta¨tt, Germany. REISZ,R.R.,AND H.-D. SUES. 2000. The ‘feathers’ of MARTIN,L.D.,AND S. A. CZERKAS. 2000. The fossil Longisquama. Nature 408:428. record of feather evolution in the Mesozoic. RICQLE` S,A.J.D., K. PADIAN,J.R.HORNER, AND H. American Zoologist 40:687–694. FRANCHILLON-VIEILLOT. 2000. Paleohistology of MARTIN,L.D.,AND J. D. STEWART. 1985. Homologies the bones of pterosaurs (Reptilia: Archosauria): in the avian tarsus. Nature 315:159. Anatomy, ontogeny, and biomechanical impli- MARTIN,L.D.,J.D.STEWART, AND K. N. WHETSTONE. cations. Zoological Journal of the Linnean Soci- 1980. The origin of birds: Structure of the tarsus ety 129:349–385. and teeth. Auk 97:86–93. RIEPPEL, O. 1993. Studies on skeletal formation in NORELL,M.,Q.JI,K.GAO,C.YUAN,Y.ZHAO, AND reptiles. IV. The homology of the reptilian (am- L. WANG. 2002. Dinosaur feathers. Nature 416: niote) astragalus revisited. Journal of Vertebrate in press. Paleontology 13:31–47. NORELL,M.,P.J.MAKOVICKY, AND J. M. CLARK. 1998. RUBEN,J.A.,AND T. A. JONES. 2000. Selective factors A Velociraptor wishbone. Nature 389:447. associated with the origin of fur and feathers. OSTROM, J. H. 1974. Archaeopteryx and the origin of American Zoologist 40:585–596. flight. Quarterly Review of Biology 49:27–47. RUBEN,J.A.,T.A.JONES,N.R.GEIST, AND W. J. H IL- PADIAN, K. 2001. Cross-testing adaptive hypotheses: LENIUS. 1997. Lung structure and ventilation in Phylogenetic analysis and the origin of bird theropod dinosaurs and early birds. Science 278: flight. American Zoologist 41:598–607. 1267–1270. PADIAN,K.,AND L. M. CHIAPPE. 1997. Bird origins. SCHWEITZER,M.H.,J.A.WATT,R.AVCI,L.KNAPP, Pages 71–79 in Encyclopedia of Dinosaurs (P. J. L. CHIAPPE,M.NORELL, AND M. MARSHALL. Currie and K. Padian, Eds.). Academic Press, 1999. Beta-keratin specific immunological reac- San Diego, California. tivity in feather-like structures of the Cretaceous PADIAN,K.,AND L. M. CHIAPPE. 1998. The origin and alvarezsaurid, Shuvuuia deserti. Journal of Exper- early evolution of birds. Biological Reviews 73: imental Zoology (Molecular and Developmental 1–42. Evolution) 285:146–157. PADIAN,K.,A.J.D.RICQLE` S, AND J. R. HORNER. 2001. SERENO, P. 1997. The origin and evolution of dino- Dinosaurian growth rates and birds origins. Na- saurs. Annual Review of Earth and Planetary ture 412:405–408. Science 25:435–489. PATTERSON, C. 1982. Morphological characters and SERENO, P. 1999. The evolution of dinosaurs. Science homology. Pages 21–74 in Problems in Phylo- 284:2137–2147. genetic Reconstruction (K. A. Joysey and A. E. STOKSTAD, E. 2001. Exquisite Chinese fossils add Friday, Eds.). Academic Press, London. new pages to book of life. Science 291:232–236. PERRY, S. F. 2001. Functional morphology of the rep- SUES, H.-D. 2001. Ruffling feathers. Nature 410:1036– tilian and avian respiratory systems and its im- 1037. plications for theropod dinosaurs. Pages 429– SUMIDA,S.S.,AND C. A. BROCHU. 2000. Phylogenetic 441 in New Perspectives on the Origin and Early context for the origin of feathers. American Zo- Evolution of Birds (J. Gauthier and L. F. Gall, ologist 40:486–503. January 2002] Perspectives in Ornithology 17

TARSITANO, S. F. 1985. The morphological and aero- WILLISTON, S. W. 1879. Are birds derived from di- dynamic constraints on the origin of birds and nosaurs? Kansas City Review of Science 3:457– avian flight. Pages 319–332 in The Beginnings of 460. Birds (M. K. Hecht, J. H. Ostrom, G. Viohl, and WITMER, L. M. 1991. Perspectives on avian origins. P. Wellnhofer, Eds.). Freunde des Jura-Museum, Pages 427–465 in Origins of the Higher Groups Eichsta¨tt, Germany. of Tetrapods (H.-P. Schultze and L. Trueb, Eds.). UNWIN,D.M.,AND M. J. BENTON. 2001. Longisquama Cornell University Press, Ithaca, New York. fossil and feather morphology. Science 291: XU, X., Z.-L.TANG, AND X.-L.WANG. 1999b. A ther- 1900–1901. izinosauroid dinosaur with integumentary VARRICCHIO,D.J.,F.JACKSON, AND C. N. TRUEMAN. structures from China. Nature 399:350–354. 1999. A nesting trace with eggs for the Creta- XU, X., X.-L.WANG, AND X.-C. WU. 1999a. A dro- ceous theropod dinosaur Troodon formosus.Jour- maeosaurid dinosaur with a filamentous integ- nal of Vertebrate Paleontology 19:91–100. ument from the Yixian Formation of China. Na- VOGEL, G. 1997. Forensic science: Phylogenetic anal- ture 401:262–266. ysis: Getting its day in court. Science 275:1559– XU,X.,Z.ZHOU, AND R. O. PRUM. 2001. Branched in- 1560. tegumental structures in Sinornithosaurus and AGNER AND AUTHIER ϭ W ,G.P., J. A. G . 1999. 1,2,3 the origin of feathers. Nature 410:200–204. 2,3,4: A solution to the problem of the homology XU,X.,Z.ZHOU, AND X. WANG. 2000. The smallest of the digits in the avian hand. Proceedings of known non-avian theropod dinosaur. Nature the National Academy of Sciences USA 96:5111– 408:705–708. 5116. ZHOU, Z. 1995. Is Mononychus a bird? Auk 112:958– WALKER, A. D. 1972. New light on the origin of birds and crocodiles. Nature 237:257–263. 963. ZHOU, Z. 2000. Caudipteryx and the origin of flight in WELLNHOFER, P. 1985. Remarks on the digit and pubis problem of Archaeopteryx. Pages 113–122 in birds. Vertebrata PalAsiatica 38(Supplement):38. The Beginnings of Birds (M. K. Hecht, J. H. Os- ZHOU,Z.,AND X.-L. WANG. 2000. A new species of trom, G. Viohl, and P. Wellnhofer, Eds.). Freunde Caudipteryx from the Yixian formation of Liaon- des Jura-Museum, Eichsta¨tt, Germany. ing, northeast China. Vertebrata PalAsiatica 38: WELMAN, J. 1995. Euparkeria and the origin of birds. 113–127. South African Journal of Science 91:533–537. ZHOU, Z., X.-L. WANG, AND X. XU. 2000. Important WHETSTONE,K.N.,AND L. D. MARTIN. 1981. New features of Caudipteryx—Evidence from two look at the origin of birds and crocodiles. Nature nearly complete new specimens. Vertebrata 279:234–236. PalAsiatica 38:241–254.