TECHNICAL COMMENTS Counting the Fingers of Birds and Dinosaurs favor the I-II-III hypothesis. The shift of the axis may be linked to the ossification of the distal carpal elements, which may have Homologies of the three fingers in birds cia is based on the “ground-plan” of the caused perturbation of the distal branching have been debated for more than a century. hand of living tetrapods (alligators, for ex- pattern by modification of the expression Paleontologists have traditionally identified ample) in which digit IV always appears domains of the Hox D genes (5). That the avian digits as I-II-III largely on the basis of first during development. In the case of ulnare is supposed to part of the primary phalangeal counts, whereas embryologists digital reduction, however, the correspon- axis, but is lost during avian ontogeny (7), number them II-III-IV on the basis of de- dence between primary axis and digit IV is strong evidence for perturbation of the velopment in the egg. The report by Ann appears to break down. For example, in primary axis in birds. C. Burke and Alan Feduccia (1)isasyn- salamanders, the first digit to form is digit Developmental biologists have used oth- thesis of the embryological evidence. They II, not digit IV (5). Burke and Feduccia er criteria to support the II-III-IV hypothe- observe that in most amniotes, the first acknowledge that the loss of digit IV in sis, such as the topographic position of the digit to form in the pentadactyl manus is theropod evolution was unusual and does pisiform and the sequence of chondrogene- digit IV, which develops a “primary axis.” not follow the general rule of hand devel- sis. Hinchliffe (7) identifies five precartilag- With the use of this developmental con- opment. Furthermore, digit IV was absent inous elements in developing chicks: the straint, they identified the primary axis in in two-fingered Tyrannosaurus (I-II) and radiale, ulnare, distal carpal 3 (semilunate birds as digit IV, and the surviving digits as one-fingered Mononykus (I), which reveals bone), X, and pisiform. He regards two II-III-IV. This conclusion is incompatible the shortcoming of the rule. If birds are proximal carpals as the pisiform and the with theropod (dinosaur) ancestry of birds members of theropods (3–4), the presence radiale. He states that the true ulnare re- because theropod digits are identified as of digit IV in Archaeopteryx and adult birds gressesduringdevelopmentandisreplaced I-II-III, with vestigial fourth and fifth digits is doubtful. It would be difficult to argue by a new “element X” of uncertain affinity. apparent in the fossil record. The origin of that later birds re-evolved digit IV, while Because the pisiform occurs laterally and birds from dromaeosaurid-like theropods is losing digit I, regardless of the pattern of adjacent to the fifth metacarpal in primitive supported by a large suite of synapomor- development. It is more likely that, over archosaurs, the rudimentary metacarpal in phies, and thus has achieved wide accep- eons, the primary axis shifted its position in the chick’s wing is identified as digit V, and tance (2–4). Burke and Feduccia apparently concert with the reduction of digits. Shubin the rest as digits IV, III, and II. regard these similarities as convergence, not (6) proposed that the primary axis in birds It appears that in Hinchliffe’s interpre- homology. may actually represent digit III because of tationgreatweightisgiventothepisi- The interpretation of Burke and Feduc- developmental acceleration, which would form’spositionforidentifyingdigits.Ina

Fig. 1. Left manus of selected theropods in a phylogenetic context (2, 4) compound distal carpal (shown in stippled) support the idea that the surviving shows the pattern of digital reduction and the evolution of wrist from universal digits of maniraptoran dinosaurs and birds are I-II-III and that the semilunate joint to swivel joint. Phalangeal counts and the topographic relationship of the bone represents fused distal carpals 1 and 2.

www.sciencemag.org ⅐ SCIENCE ⅐ VOL. 280 ⅐ 17 APRIL 1998 355a pentadactyl manus, the pisiform occurs ad- carpal becomes the semilunate carpal in 3. J. Gauthier, Mem. Calif. Acad. Sci. 8, 1 (1986). jacent to the fifth metacarpal, but this maniraptorans, which allows a swivel wrist 4. S. Chatterjee, The Rise of Birds (Johns Hopkins Univ. Press, Baltimore, MD, 1997). relationship is tenuous in other animals joint. The topographic relationship of the 5. N. Shubin and P. Alberch, Evol. Biol. 20, 319 (1986). with the loss of postaxial digits. Because semilunate bone suggests that the surviving 6. N. Shubin, in Interpreting the Hierarchy of Nature,L. the pisiform occurs in the proximal row of digits of maniraptorans are I-II-III (Fig. 1). Grande and O. Rieppel, Eds., (Academic Press, San the carpus, its topographic relation with If so, Ostrom’s “radiale” actually represents Diego, CA, 1994), pp. 201–225. 7. J. R. Hinchliffe, in The Beginnings of Birds,M.K. the lateral metacarpal is not direct. It will distal carpals 1 and 2, whereas the true Hecht, J. H. Ostrom, G. Viohl, P. Wellnhofer, Eds. always occur lateral to the ulnare, irre- radiale and ulnare are not yet known from (Freunde des Jura-Museuns Eichsta¨ tt, Eichsta¨ tt, spective of loss of any digits. If so, the the wrist of Deinonychus. Synthesis of both West Germany, 1985), pp. 141–147. 8. L. D. Martin, in Origins of the Higher Groups of Tet- embryological convention that digit I is neontological and paleontological data sug- rapods: Controversy and Consensus, H.-P. Schultze missing is not based on firm evidence. gests that the surviving avian digits are and L. Trueb, Eds. (Cornell Univ. Press, Ithaca, NY, Paleontologists have used two lines of I-II-III, and thus supports their theropod 1991), pp. 485–540. evidence to support the I-II-III hypothesis: origin. 9. A. Feduccia, The Origin and Evolution of Birds (Yale Univ. Press, New Haven, CT, 1996). (i) conserved phalangeal formulae (2–4) and Sankar Chatterjee 10. P. C. Sereno, J. Vert. Paleont. 13, 425 (1993). (ii) topographic relationship of the semilu- Museum of Texas Tech University, 11. ࿜࿜࿜࿜, C. A. Forster, R. R. Rogers, A. M. Monetta, nate carpal with the corresponding metacar- Lubbock, TX, 79409–3191, USA Nature 361, 64 (1993). pals. The plesiomorphic phalangeal count 12. E. H. Colbert, Bull. Mus. North. Arizona 57, 1 (1989). 13. I thank N. Shubin, N. Hotton, and L. M. Witmer for for archosaurs is 2-3-4-5-3. Many archosaur REFERENCES AND NOTES reading the manuscript and M. W. Nickell for illustra- lineages have a reduced number of digits, but ______tion. K. Ohsugi and J. R. Hinchliffe have kindly shared have retained the original phalangeal formu- 1. A. C. Burke and A. Feduccia, Science 278, 666 their ideas. Supported by Texas Tech University. (1997). la in the digits that remain. The three digits 2. J. H. Ostrom, Biol. J. Linn. Soc. 8, 91 (1976). 24 November 1997; accepted 25 February 1998 of dromaeosaurs and Archaeopteryx have the same phalangeal formula of 2-3-4 as digits I, II, and III of basal archosaurs. Thus, the Burke and Feduccia conclude (1) that the hand are equivalent. Because these assump- reduction of the digits in maniraptorans is development of the avian hand is incom- tions are not correct for theropod dinosaurs, believed to have occurred from the posterior patible with a dinosaurian ancestry of birds. Burke and Feduccia have effectively as- to the anterior side with the loss of digits V This conclusion, however, does not fit the sumed that birds are not dinosaurs, and the and IV. The pattern of digital reduction data; the theropod manus has a unique and report’s conclusion that they are not inev- becomes apparent from the phylogenetic hi- extraordinary pattern of digit reduction (1, itably follows irrespective of the results of

erarchy of theropods (Fig. 1). By extension, 2) that must be based on a derived pattern the experiments in the report, or of evolu- modern birds also possess digits I-II-III, but of development. The identification by tionary history. Furthermore, these assump- show further reduction of several phalanges Burke and Feduccia (1) of the posterior tions appear tautological—they are not in- during evolution. digit in the avian hand as digit IV is based dependent of each other, nor of the conclu- The identity of the semilunate carpal on the assumptions that digit IV is the first sions reached in the report. provides an additional clue to the number- to develop, that the pattern of development Shublin and Alberch (3) demonstrated ing of theropod digits. Ostrom (2) misiden- in the avian hand is not extraordinary, and that the ontogeny of all tetrapod limbs fol- tified this bone in maniraptorans as “radi- that the development of the avian foot and lows the same stereotypic pattern. Carpal ale” instead of distal tarsal and initiated the confusion. Critics (8, 9) pointed out that this bone cannot be homologous with the avian semilunate bone because the latter is a distal carpal, and thus questioned the theropod ancestry of birds. However, the articulation of the semilunate carpal in ma- niraptorans with corresponding metacarpals indicates that the bone in question (2) must be distal carpal, not proximal radiale, con- trary to Ostrom’s idea (3). The identifica- tion of the bone can be further resolved in a phylogenetic context. In Herrerasaurus (10), the manus is pentadactyl; the wrist shows two proximal carpals (the radiale and ulnare), one centrale, and four distal carpals (one for each inner metacarpal, I-IV). Metacarpal V is reduced and lacks its distal carpal. In Eoraptor (11) and Coelophysis Fig. 1. (A) Development of the amniote hand. Elements developing from the radius are omitted for (12), the next stage of manual modification clarity. Bones develop from condensations of cartilage, that arise either de novo, from a Y-shaped can be seen; the distal carpal is integrated branching event of another condensation, or from the distal budding of a cartilage condensation. Ulna into a compound bone that receives meta- gives rise to the intermedium (i), and the ulnare (ul), which in turn branches to produce a centrale (absent carpals I and II, respectively. It must repre- in crocodiles and dinosaurs) and the carpal IV (c4). Carpal IV then branches to produce metacarpal IV (and hence digit IV ), and carpal III (c3), a process which is reiterated to generate the digital arch and sent distal carpals 1 and 2. The fifth meta- further digits. Digit V arises from the de novo condensation of metacarpal V posterior to the ulnare (3). carpal is lost. Now that the homology of With the exception of theropods, digit loss occurs progressively from the anterior end of this chain (digit this compound bone is ascertained, it can I), and from the isolated loss of digit V. (B) Development of the hand in early theropods. In the early be traced across the phylogeny of theropods, theropod Coelophysis bauri, digit V is lost, carpals I and II are fused, reduction of digit IV is not yet allowing us to number the digits. The distal complete, and the carpal and metacarpal can be seen (2). Dashed lines indicate lost or fused elements.

www.sciencemag.org ⅐ SCIENCE ⅐ VOL. 280 ⅐ 17 APRIL 1998 355a TECHNICAL COMMENTS

Fig. 2. Possible developmental programs responsible for the theropod Ulnare branches to produce carpal IV, which gives rise to carpal III, but hand. Labels as in Fig. 1. (A) Carpal IV condensation is progressively remains fused to it. (C) Ulnare gives rise to carpal IV, which remains fused reduced, until the branching of the ulnare gives rise directly to carpal III. (B) to the ulnare.

IV is the developmental cornerstone of the next carpal element in the digital arch; the The developmental aspects of the avian hand: its Y-shaped branching to produce first digit would be digit III, not IV, as in all hand reported by Burke and Feduccia are, digit IV and carpal III initiates the digital other tetrapods (1). Burke and Feduccia’s despite their conclusion to the contrary, arch (Fig. 1). The loss of digit IV and its identification of this first digit as IV is based entirely consistent with a theropod origin of associated carpal elements (2) makes the on the assumption that the first digit to birds. theropod manus extraordinary, for without develop is digit IV in birds as well as other Joseph P. Garner carpal IV the remaining digits could not tetrapods, but this is the very hypothesis Adrian L. R. Thomas develop. The unique and extraordinary pat- that they are testing. Department of Zoology, tern of digit reduction in theropods implies Furthermore, Shubin and Alberch (3) Oxford University, a unique developmental pattern. describe a unique pattern of development South Parks Road, In later theropods, digit IV is completely for digit V in birds. In all other tetrapods, Oxford OX1 3PS, United Kingdom reduced, and carpal IV is lost. In develop- digit V arises from a de novo condensation, E-mail: [email protected] ment, however, the digital arch must either but in birds it arises from a Y-shaped REFERENCES pass through the cartilaginous precursor of branching of the ulnare, exactly as if carpal ______carpal IV or be initiated with carpal III. IV does not separate from the ulnare (Fig. 1. A. C. Burke and A. Feduccia, Science 278, 666 Because carpal IV is not visible in the 2C). Labelling the posterior, transient digit (1997). theropod wrist, its cartilaginous precursor as V rather than IV would require a funda- 2.A.Feduccia,TheOriginandEvolutionofBirds(Yale must be subsumed within, or fused to, carpal mental rewriting of the developmental pro- Univ. Press, New Haven, CT, 1996), pp. 68–71. III or the ulnare (Fig. 2). In either case, the gram, with the ulnare producing a trifurca- 3. N. Shubin and P. Alberch, Evol. Biol. 20, 319 (1986). 4. J. A. Gauthier, Mem. Calif. Acad. Sci. 8, 1 (1986). ulnare would give rise to a distal condensa- tion, the most anterior branch of which has tion, which branches to form a digit and the been suppressed. 1 December 1997; accepted 25 January 1998

Response: The identification in the report cladogram one favors. The convergence, to). The polarity of this character in

(1) of the digits of the avian hand as II-III- wherever it may lie, is at least as interesting salamanders as opposed to frogs and am- IV is based on a highly conserved pattern of and important as the homologies, and de- niotes has even lead to hypothesis about the development among amniotes (Fig. 1) and serves attention. paraphyly of the Lissamphibia. is at odds with a proposed theropod origin Chatterjee mentions that “the corre- The characteristic pattern we describe in of birds. The comments by Chatterjee and spondence between primary axis and digit the report involves early cartilaginous con- by Garner and Thomas argue that the IV appears to break down” in salamanders, densations that form the anlagen of the reigning hypothesis of avian origins renders for example. This is correct, and for this skeleton during development. Actual ossi- our developmental interpretation impossi- reason we have limited our comparison to fication occurs long after the initial pattern ble. Chatterjee cites the large number of amniote patterns. It is also correct, in this forming stages, and subsequent patterns of synapomorphies uniting birds and regard, that the unusual mode of develop- fusion do not always reflect the original dromeosaurid-theropods and then states ment of the urodele hand and foot is a cartilaginous pattern. Therefore, without “Burke and Feduccia apparently regard precedent for alteration in developmental reversing causality, it is difficult to see how these similarities as convergence, not ho- patterns. Salamanders are a remarkable ex- ossification of distal carpal elements could mology.” Such a statement was not made in ception. They do not represent a “simple” have an effect on a more rudimentary stage the report (1), although it was discussed in variation wherein the primary axis shifts to to the degree of shifting a developmental the accompanying Perspective (2). Howev- extend through digit II, as implied by Chat- axis. The ulnare is present in avian embryos er, this criticism highlights an important terjee. Salamanders violate the proximal to as a precartilagenous element that can be aspect of our discussion. Convergence will distal pattern exhibited by all other tetra- seen between the condensation of the ulna be present in some characters, whichever pods and have no primary axis (sensu stric- and a distal element that represents distal

www.sciencemag.org ⅐ SCIENCE ⅐ VOL. 280 ⅐ 17 APRIL 1998 355a alteration on the stereotyped pattern we digits based on the conservation of devel- describe for amniotes. A radical change is opmental patterns seen in amniotes. To certainly possible, but not necessary. The say that this pattern remains exactly the theropod hand is unusual, not because of same in birds and other amniotes, except the loss of digit IV, but because of the loss of for the numbering of the digits, would digit IV accompanied by the retention of seem to require “special pleading” and digit I. It is the latter character that is most would be inconsistent with the observa- significant. We suggest that it is possible tions and current evidence of comparative that the theropod hand developed in a fash- embryology. The relationship of birds and ion consistent with the early developmental dinosaurs is an hypothesis, and our report pattern in other amniotes, with a primary points out an inconsistency in this popular axis running through digit IV. Subsequently idea. during development, digit IV is totally re- Ann C. Burke duced. As mentioned in our report, there J. Alan Feduccia are several extant lizards that have almost Department of Biology, completely reduced digit IV [see the refer- University of North Carolina, ences in (3)]. Chapel Hill, NC 27599–3280, USA The other issue raised by Garner and E-mail: [email protected] Thomas involves the development of digit Richard Hinchliffe V. In snapping turtles and alligators, digit V Institute of Biological Sciences, appears as a de novo condensation. Garner University of Wales, and Thomas cite the appearance of digit V Aberystwyth, as a branch off of the postaxial carpal ele- Cardiganshire SY23 3DA, United Kingdom Fig. 1. Early chick left forelimb bud showing the ment in chicks as evidence that it must E-mail: [email protected] primary axis, which corresponds to digit IV. Image actually be digit IV. In fact, digit V devel by S. Whitfield. - ops with strong connectivity to the postax- REFERENCES ial carpal in mammals and in lizards, so a de ______carpal and metacarpal IV. The fact that its novo appearance does not diagnose this 1. A. C. Burke and A. Feduccia, Science 278, 666 individual identity is then obscured by later digit. (1997). regression does not eliminate its initial sig- In sum, one can argue that the primary 2. R. Hinchliffe, ibid., p. 596. nificance based on connectivity. axis shifted in birds and theropods during 3. A. Raynaud, in Biology of the Reptiles, C. Gans and Garner and Thomas center their criti evolution, but at present there is no de- F. Billett, Eds. (Wiley, New York, 1985), vol. 15, pp. - 61–148. cism on the fact that the theropod hand is velopmental data to support such a model. highly unusual and must represent a total We have made our identification of avian 1 December 1997; accepted 25 February 1998

www.sciencemag.org ⅐ SCIENCE ⅐ VOL. 280 ⅐ 17 APRIL 1998 355a