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Commentary

The Auk 120(2):550–561, 2003

ARE CURRENT CRITIQUES OF THE THEROPOD ORIGIN OF SCIENCE? REBUTTAL TO FEDUCCIA (2002)

RICHARD O. PRUM1 Department of Ecology and Evolutionary , and Natural History Museum, University of Kansas, Lawrence, Kansas 66045, USA

INMYPerspectives in essay (Prum unknown early archosaurian ancestor and are 2002), I advocated that all ornithologists should unrelated to theropod . be excited about research on the theropod origin Rather than specifi cally counter the problems of birds. Although I did address some criticisms with his commentary, I think it would be most of the theropod hypothesis, I spent most of the productive to focus my response on the intel- essay outlining the data in support of the thero- lectual framework of Feduccia’s critique of the pod origin and, most exciting to me, describing theropod . Specifi cally, I will ask the new directions in evolutionary ornithological the question, “Is this science?” Or is it merely research that have opened up as a consequence. a form of rhetoric designed support an a priori I concluded that one of the most important fron- belief about evolutionary process and history? tiers in ornithological research in this century will be the establishment of a thorough scientifi c THE INTELLECTUAL STRUCTURE OF understanding of the of avian biology FEDUCCIA’S CRITIQUE in light of the theropod origin of birds. From nesting biology and physiology to behavior and A critical element of science is falsifi ability. locomotion, the rewards of studying ornithol- To be scientifi c, a hypothesis must be falsifi able ogy as extant biology are only just and yield predictions that are objectively test- beginning to be reaped (Prum 2002). able. In a historical science like evolutionary In his critique of my essay, A. Feduccia (2002) biology, such tests cannot be conducted experi- reviewed much of his previous work but also mentally. However, we can analyze available sprang a new, surprise ending. In summary, evidence with objective repeatable methods. he hypothesized that birds evolved from an Another critical feature of science is the pro- unknown lineage of early , and posal of alternative hypotheses or theories that that rampant renders the attempt to explain the scientifi c data at hand. many derived morphological characters shared Does Feduccia’s critique meet these minimal by birds and theropods unreliable. However, criteria of science? Feduccia can no longer deny the conclusive evi- Feduccia (2002) offers an alternative to the the- dence that basal dromaeosaurs had (Xu ropod hypothesis of origins that is so vague et al. 1999, 2000, 2001, 2003; Czerkas et al. 2002; as to be literally untestable. When Heilmann Norell et al. 2002). In the end, he concedes that (1926) fi rst proposed the basal hypoth- dromaeosaurs had feathers. In a rhetorical tour esis of avian origins, he described it optimistical- de force that confl icts with decades of his own ly as “wholly without short comings.” Similarly, work and most of his commentary, Feduccia Feduccia (2002) describes his hypothesized early (2002) then hypothesizes that dromaeosaurs ancestral archosaurian lineage as having “less are birds, but that the birds, now including specialized anatomical baggage” than theropod the dromaeosaurs, still originated from some dinosaurs. This ancestral tabula rasa hypothesis has survived the intervening 75 years between them only because it is permanently immune 1 E-mail: [email protected] to falsifi cation. Any potential character confl icts 550 April 2003] Commentary 551 between birds and any known archosaurs can be to avoid dealing with the overwhelming volume rejected as irrelevant because the specifi c organ- of character evidence from all parts of the body isms can be claimend to not actually represent supporting the theropod origin. He frequently the yet unknown, hypothetical ancestor that argues both sides of the same issue wherever perfectly conforms to the theory. Feduccia’s ad- it is convenient. For example, when the fi rst vocacy of an unfalsifi able alternative hypothesis nonavian theropod was described for violates a fundamental tenet of science, but it (Norell et al. 1998), Feduccia and also permits him to continue his permanent rhe- Martin (1998) claimed that the presence of a fur- torical battle against the theropod hypothesis of cula in the basal archosauromorph avian origin. demonstrates that those structures have evolved In response to my request for an explicit al- multiple times in archosaurs and are “weak ternative hypothesis of avian origin, Feduccia evidence” of phylogenetic relationship. Now, (2002) concluded that “there are times when applying his “character by character” approach there is insuffi cient evidence to make the for- in this commentary, Feduccia mentions that the mulation of a hypothesis feasible.” Here, he is furcula of Longisquama in an effort to support the not actually engaged in the search for a scien- hypothesis that Longisquama is closely related to tifi c solution to the question of avian origins. birds, in direct contradiction to his earlier pub- Essentially, Feduccia concedes that he would lished conclusions. Simultaneously, he ignores rather not do science (i.e. formulate and test the discoveries since 1998 of furculae or paired alternative hypotheses with data) than to accept in six to nine major lineages of theropod the theropod origin of birds. Unfortunately, dinosaurs, including dromaeosaurs, ovirap- Feduccia’s rejection of the theropod hypothesis tors, tyrannosaurs, allosaurs, and coelophysids and advocacy of an untestable alternative does (Tykoski et al. 2002). Of course, the only scientifi c not constitute a scientifi c explanation of the ori- way to resolve alternative hypotheses of charac- gin of birds. ter evolution and character confl icts are by ap- Feduccia (2002) also claims that “phylogenet- plying a repeatable, explicit, analytical method ic stands alone among the sciences” to reconstruct evolutionary history of characters in demanding that critics propose a testable and organisms. But Feduccia (2002) openly re- alternative hypothesis. But, as Thomas Kuhn jects available systematics methods as forcing (1970:77) wrote, “The decision to reject one “into algorithmic form what is arguably the most paradigm is always simultaneously the decision subjective and qualitative fi eld of biology.” to accept another, and the judgment leading to Feduccia’s (2002) dogmatic belief in ram- that decision involves the comparison of both pant evolutionary convergence in morphology paradigms with nature and with each other.” literally begs the question—that is, presumes What Feduccia rejects as the irrational demands exactly the facts that need to be demonstrated. of phylogenetic zealots are actually the baseline The only way to demonstrate convergence is to requirements of all sciences, from astrophysics show that the majority of character evidence to . supports a hypothesis of phylogeny in which Because Feduccia’s scenario is untestably the convergent characters are shown to have vague, he is reduced exclusively to criticizing the evolved independently (Patterson 1982, Pinna theropod hypothesis. Feduccia (2002) portrayed 1991). Yet, Feduccia rejects both repeatable the theropod origin of birds as a vast cladisitic systematic methods and explicit, testable al- conspiracy to deceive the ornithological com- ternative hypotheses, making it impossible for munity. Like a conspiracy theorist, he unerringly him to demonstrate the convergence in which interprets evidence—even the new, ultimate he believes. Feduccia (1999a,b; 2002) repeatedly evidence of feathered theropods—as favoring cited his favorite examples of failed phyloge- his preconceived conclusions. Feduccia (2002) netic hypotheses as a justifi cation for rejecting argues that hypotheses of character repeatable scientifi c methods, but he failed to cannot be tested by congruence with other char- mention that it was subsequent phylogenetic acters, advocating a character by character ap- analyses that established the preferred hypoth- proach instead. This ad hoc method permits him eses. Actually, the repeatable scientifi c methods to interpret each separate character in whatever that Feduccia rejects are the solution, not the manner he prefers to support his argument, and problem. Feduccia (2002) further states that 552 Commentary [Auk, Vol. 120 the theropod hypothesis implies that drom- tion of the temporal paradox by two thirds (Xu aeosaurs are “avian ancestors,” and that bird et al. 1999, 2000, 2001, 2003; Czerkas et al. 2002; are “derived from dromaeosaurs,” when it is Norell et al. 2002), bird-like nesting behavior in well known that the hypothesis states that the theropods (reviewed in Prum 2002), and most birds and dromaeosaurs (probably including recently by four winged dromaeosaurs (Xu et al. troodontids) are sister groups. 2003). Given that the theropod origin of birds is Feduccia has long maintained that the 80 Ma entirely consistent with and supported by all of “temporal paradox”—the temporal gap in fos- the new evidence discovered in the last decade, sil record between the earliest bird and and that many testable predictions generated the earliest fossils of the proposed avian sister by the hypothesis have been independently (dromaeosaurs and troodontids)—was a supported, it is an overwhelmingly successful problem for the theropod hypothesis. Recent scientifi c theory. discoveries have now uncovered basal drom- Lastly, Feduccia (2002) advocated the no- aeosaurs that are 124–128 Ma old (Xu et al. 1999, tion that convergent evolution may make the 2000, 2001, 2003; Czerkas et al. 2002; Norell et ancestry of birds unknowable. Given the de- al. 2002) cutting the proposed temporal para- tailed support for the theropod hypothesis, that dox to 25 Ma or less, and fulfi lling a specifi c view is unscientifi c, and reveals a fundamental prediction of the theropod hypothesis. Feduccia weakness of Feduccia’s critique. Feduccia (2002) (2002) responded that the reduction of the gap quoted Scottish philosopher David Hume as is unimpressive because it is now “equally writing in favor of natural laws. However, probable that early birds are much earlier than Hume is actually better known for his skeptical .” Feduccia’s faith in this gap is so critique of the existence of all empirical knowl- strong that in response to new evidence reduc- edge. Hume argued that inductive knowl- ing the supposed temporal gap by more than edge—conclusions based on observations and two thirds, he argued for a new increase in the experiment—is only valid if natural processes gap because birds must now be substantially are uniform over time, but that any evidence of older than Archaeopteryx. Further, Feduccia such uniformitarianism is necessarily based on (2002) ignored the evidence from Brochu and inductive observation, making the entire enter- Norell (2000) that his preferred basal archosaur prise of science a circular fallacy. Like Hume, origin of birds requires hypothesizing even Feduccia rejects the overwhelming empirical longer “ghost lineages” than does the theropod evidence of theropod hypothesis of the origin hypothesis. of birds because he views the methods used to Feduccia (2002) also tried to characterize establish it as inherently circular and fl awed. my enthusiasm for the theropod origin as “the Although Hume’s eighteenth-century criticisms zeal of new school cladism.” Actually, my en- of science are philosophically irrefutable, they thusiasm is not based on ideological zeal, but have not prevented science from progressing on the incomparable scientifi c success of the substantially in the last 300 years. Likewise, theropod hypothesis (Prum 2002). Since it was the undeniable success of the theropod origin fi rst proposed cladistically by Gauthier (1986), hypothesis in explaining the data and predict- the theropod origin of birds has been supported ing new discoveries from , devel- by numerous discoveries, including many new opmental biology, and functional morphology theropods closely related to birds (Novas and is the ultimate, eloquent response to Feduccia’s Puerta 1997; Sereno 1999; Xu et al. 1999, 2000, philosophical rejection of objective systematic 2001, 2003; Czerkas et al. 2002; Norell et al. methods. 2002), many new basal avian fossils that further blur the distinction between birds and other DROMAEOSAURS ARE BIRDS? theropods (Forster et al. 1998; Zhou and Zhang 2002), many theropod furculae (Tykoski et al. Could anyone imagine better evidence that 2002), over a dozen feathered theropods (Prum birds evolved from a lineage of theropod and Brush 2002), the frameshift hypothesis dinosaurs than the presence of modern, pen- (Wagner and Gauthier 1999), and molecular naceous feathers in the theropod dinosaur developmental support for the frame-shift lineage that was independently hypothesized (Dahn and Fallon 2000)(see below), the reduc- to be most closely related to birds? In the last April 2003] Commentary 553

FIG. 1. gui, a basal dromaeosaur with a head and feathered body and asymmetrical pennaceous flight feathers extending from its , legs, and tail (Xu et al. 2003). The presence of elongate feathers on the hind limbs are confirmed independently by two other finds (Czerkas et al. 2002, Norell et al. 2002). Xu et al. (2003) hypothesize that avian flight evolved initially through a gliding, four winged morphology (represented by this four-winged basal dromaeosaur), and that the hind wings were lost in the ancestor of birds with the evolution of a powered forewing flight stroke (Prum 2003). (Photo courtesy of X. Xu and Z. Zhou.) couple of years, there has been an avalanche After maintaining that feathered theropods of nonavian theropod specimens from were a “myth” or “artistic inventions” (Feduccia Liaoning, China with a variety of fi lamentous 1999a), and stating in his commentary that integumentary appendages including fully he cannot fi nd “any credible evidence” of the pennaceous modern feathers on multiple speci- existence of theropod feathers, Feduccia (2002) mens of dromaeosaurs (reviewed in Prum and completely capitulates and concluded, “There Brush 2002). Most recently, three papers have are also asymmetric fl ight feathers preserved on demonstrated perfectly pennaceous feathers on the and near the hind limbs of a dromaeo- basal dromaeosaurs from the Liaoning (Czerkas saurid (Czerkas et al. 2002, Norell et al. 2002).” et al. 2002; Norell et al. 2002; Xu et al. 2003) . How does Feduccia integrate those new dis- Since Feduccia (2002), Xu et al. (2003) have pub- coveries into his anti-dinosaur-origin rhetoric? lished the description of Microraptor gui, a basal Tellingly, he alters only the smallest necessary dromaeosaur with perfectly pennaceous, asym- details of his scenario, he concedes no contra- metrical modern fl ight feathers on its tail, arms, diction with his decades of previous writings and legs (Fig. 1). Previous specimens published and most of this commentary, and he concludes by Czerkas et al. (2002: fi gs. 1, 11) and Norell et the same thing. He writes, “we must now care- al. (2002) independently confi rm the presence of fully consider the possibility that there may long pennaceous leg feathers in basal dromaeo- have been a number of radiations of secondarily saurs. Those descriptions confi rm the existence fl ightless birds that evolved mor- of pennaceous feathers in exactly the lineage of phologies quite similar to theropod dinosaurs.” theropod dinosaurs hypothesized independent- That is, Feduccia (2002) hypothesizes that ly to be most closely related to birds. The thero- dromaeosaurs are birds that are extraordinarily pod hypothesis has been stunningly supported convergent with theropod dinosaurs, and that by the discovery that the most essentially avian birds, including dromaeosaurs, originated from morphological feature—feathers—evolved in an early archosaurian ancestor and are still not theropod dinosaurs prior to . closely linked to theropod dinosaurs. The ultimate evidence of the theropod origin of Feduccia (2002) concluded that the feathered birds is now a reality. dromaeosaurs should send “all those involved 554 Commentary [Auk, Vol. 120 in the debate on bird origins back to the draw- and Cryptovolans (Czerkas et al. 2002) may ing board.” He might prefer to start his argu- revolutionize our understanding of the origin ment over, given that he has spent years argu- of avian fl ight (Prum 2003). Specifi cally, wing ing that dromaeosaurs are completely unlike morphology of the four-winged theropods and unrelated to birds. It is hard to understand fulfi ll Feduccia’s (2002: fi g. 6) ideal of a gliding how he could fi nd “no credible evidence to progenitor for avian fl ight, and demonstrate justify the portrayal of the January 2002 Auk of that there is no necessary confl ict between the Microraptor with a thick, white downy coating of theropod origin of birds and a gliding origin putative protofeathers (A. Feduccia pers. obs.)” of fl ight (Chatterjee 1997, Prum 2003, Xu et al. on page 1194, and then on page 1196 admit the 2003). It appears that the avian fl ight apparatus existence of fl ight feathers on dromaeosaurs may have evolved from a combination of ter- that are Microraptor’s closest relatives. Since my restrial– that were exapted Perspectives, the description of Microraptor gui into the fl ight stroke, and subsequent selection (Xu et al. 2003) confi rms that the portrayal on for aerial gliding locomotion (Prum 2003). the January 2002 Auk was actually too conserva- Those specimens do not adversely affect the tive (Fig. 1)! Feduccia’s (2002) entire discussions hypothesis of theropod phylogeny and avian of teeth morphology and replacement, cranial origins and are perfectly good dromaeosaurs, morphology, wrist homologies (plus three complete with, for example, the “killer claw” fi gures and a table) are completely moot and on the second toe, serrate teeth, and bony sup- irrelevant given his acceptance of pennaceous porting rods in the tails. Obviously, future phy- feathers on dromaeosaurs with those serrate logenetic analyses including new data and taxa teeth, patterns of tooth replacement, cranial may change the topology of the theropod tree, morphology, and wrist . but none of those fi ndings places any doubt Feduccia’s (2002) conclusion that feathered on the placement of birds within the theropod theropods present a new challenge to all workers dinosaurs. As I concluded in my Perspectives, in the fi eld is disingenuous, because advocates the theropod hypothesis provides an increas- of the theropod origin have hypothesized that ingly detailed and coherent perspective on the dromaeosaurs were feathered for several years origin of birds. Now, the theropod hypothesis (Ji et al. 1998, 2001; Padian 1998, 2001; Prum provides new support for Feduccia’s preferred 1999; Sereno 1999; Xu et al. 2000, 2001; Norell et gliding hypothesis for the origin of fl ight, ren- al. 2002; Prum and Brush 2002). Feduccia never dering moot his frequent claim that theropods entertains the possibility that new evidence are functionally inappropriate to be avian an- fulfi lling a major prediction of the theropod cestors. origin of birds could be interpreted as defi nitive support for this hypothesis of evolutionary his- DIGIT HOMOLOGY tory. There are now more than a dozen nonavian theropods with feathers, and they belong to a As I discussed in my Perspectives, the phylo- diversity of theropod groups including ovirapto- genetic hypothesis for dinosaurs leads unam- risaurs, therizinosaurs, alvarezsaurids, and basal biguously to the conclusion that the digits of coelurosaurs (Prum and Brush 2002). If all those the bird hand are digits 1–2–3. Feduccia and feathered theropods were included in birds, as classical developmental have long Feduccia is apparently prepared to do, it would maintained that the digits of the hand of birds only contribute to the indisputable phylogenetic were digits 2–3–4 because they develop in posi- relationship between theropods and dinosaurs tions distal to the metacarpals 2–3–4 (Burke and (Prum and Brush 2002). Admitting that drom- Feduccia 1997; Feduccia 1999a, 2002). Wagner aeosaurs are feathered and closely related to and Gauthier (1999) proposed the frame-shift birds makes it impossible to argue that birds are hypothesis as a solution to the apparent confl ict. not theropod dinosaurs. The hypothesis states that theropods, including Does the discovery of asymmetrical fl ight birds, evolved to develop digits 1–2–3 distal to feathers on the and hind limbs of the metacarpals 2–3–4. dromaeosaurs affect the debate about the evo- Recent molecular developmental studies lution of avian fl ight. Doubless the four-winged have demonstrated that the simplistic position- dromaeosaurs Microraptor gui (Xu et al. 2003) al criteria and mechanistic assumptions used by April 2003] Commentary 555

Feduccia to homologize digits on the basis of to imagine are mechanistically identical to the their positions are false (Dahn and Fallon 2000, homeotic shifts in digit identity which he hy- Litingtung et al. 2002). Digit primordia are de- pothesizes are so unlikely. velopmentally naive. Identity of those primor- Feduccia demands that homeotic shifts in dia is not determined by their position relative digit identity must require a credible adap- to the metacarpals, but rather by the relative tive scenario. He overlooked that Wagner and concentration gradients of extracellular signal- Gauthier (1999) explicitly hypothesized that ing molecules in the developing hand (Dahn the frame-shift occurred through simultaneous and Fallon 2000). These data provide mechanis- for the reduction of the num- tic support the homeotic shifts in digit identity ber of digits and natural selection to maintain proposed by Wagner and Gauthier (1999). and advance the grasping function of the hand. Feduccia (2002) can no longer claim that the This hypothesis explains why theropods are a “digital mismatch between birds and dinosaurs singular exception to the pattern of digit loss is morphologically the most serious problem” common in other , which occurs as for the theropod hypothesis (Feduccia 1999a), a consequence of the reduction of digit function although he continues to try to discredit the and leads to a developmentally determined, molecular support for the frame-shift hypoth- null pattern of digit reduction. Theropods in- esis as evolutionarily outlandish and unlikely. cluding birds are a rare example of adaptive He maintains that Dahn and Fallon’s (2000) digit reduction, and that has lead to homeotic experiments yield “hopeful monsters” that are shifts in digit identity in the hand. evolutionarily irrelevant, and that the proposed Feduccia specifi cally criticizes Wagner and homeotic shifts (i.e. changes in identity among Gauthier’s (1999) hypothesis of a homeotic body parts) are undocumented in any . shift in the identity of the single wing digit of However, the evolution of vertebrae in the spi- the (Apteryx spp.) as evolutionarily inex- nal column are premier examples of homeotic plicable given its reduced function. shifts in the body. If homeotic shifts Yet, recent fi ndings on the development of digit in vertebral identity had not occurred, then identity in mice document that a single digit the homologies among vertebrae would be one morphology is the phenotype of a loss of completely obscured by evolution in vertebrae function mutant that lacks specifi c digit devel- number. opment and identity genes (Shh–/–; Gli–/+; As an alternative hypothesis, Feduccia of- Litingtung et al. 2002). A similar loss of function fers the possibility that the bird hand evolved is an entirely plausible hypothesis for through reduction in number of phalanges. He the mechanism of kiwi wing digit reduction, writes, “Reduction of phalanges is a simple and one such mechanism produces a single matter, and for Archaeopteryx… a simple sym- digit one. This molecular evidence supports the metrical reduction of one phalanx per digit plausibility of Wagner and Gauthier’s (1999) is required.” Unfortunately, this alternative homeotic shift hypothesis for the kiwi wing hypothesis is based on a distinction without digit, and further discredits Feduccia’s assump- a difference. Digit identity is defi ned by the tion that homeotic shifts must be accompanied sum total of digit phenotype, such as phalanx by strong natural selection. number and shape (Dahn and Fallon 2000). In conclusion, there are no confl icts between Experimentally, in animals like the and the theropod origin in which every digit has a distinct number of of birds. Rather, Wagner and Gauthier (1999) phalanges, digit identity is actually equivalent used the theropod origin hypothesis to make to the number of phalanges. The homeotic bold predictions about developmental biol- “hopeful monsters” that Feduccia would like us ogy that have been supported (Dahn and Fallon to fear are precisely identical to “simple” reduc- 2000). tions in the number of phalanges that Feduccia hypothesizes. Dahn and Fallon (2000) were FEATHERS studying precisely the molecular mechanisms by which the number of phalanges in a digit Alan Brush and I have recently reviewed is determined. In other words, the changes in the developmental, paleontological, and phy- phalanx number which Feduccia fi nds so easy logenetic evidence on the theropod origin of 556 Commentary [Auk, Vol. 120

feathers (Prum and Brush 2002), so I will only address a few points here. Feduccia defended the elongate scale-based model of the origins of feathers and criticizes my alternative developmental model (Prum 1999), but he fails to understand the implica- tions of our recent molecular developmental re- search on evolution (Harris et al. 2002). Along the way, he makes a number of inaccu- rate statements. First, the developmental model I proposed is not a “fi lament-to-feather” model. Rather, the model hypothesizes that feathers are fundamentally tubular, and that feathers evolved through a series of derived novelties in the developmental mechanisms within the tubular feather follicle and feather germ (Prum 1999). I hypothesized that the fi rst feathers were hollow tubes, followed by a tuft of barbs, fol- lowed by doubly branched feathers, and fi nally by feathers with a closed pennaceous vane (Fig. 2). Second, the developmental model is explicit- ly independent of all functional scenarios (Prum 1999), and is not wedded to the thermal insula- tion theory of feather origin, as Feduccia (2002) stated. However, the developmental model eas- ily falsifi es the hypothesis that feathers evolved for fl ight (Feduccia 1999b), because the fi rst feather that could have had an aerodynamic function would have required many derived developmental mechanisms (Fig. 2, Stage IV).

³

both those stages are required in the next stage. Stages IIIa+IIIb—The origin of a feather with both a rachis FIG. 2. The evolutionary transition series of feather and barbs with barbules created a bipinnate, open morphologies predicted by the developmental pennaceous structure. Stage IV—The origin of dif- theory of feather evolution (Prum 1999). The model ferentiated proximal and distal barbules created the hypothesizes the origin and diversification of feath- first closed, pennaceous vane. Distal barbules grew ers proceeded through a series derived evolutionary terminally hooked pennulae to attach to the simpler, novelties in developmental mechanisms within the grooved proximal barbules of the adjacent barb. Stage tubular feather germ and follicle. Stage I—The origin Va—Lateral displacement of the new barb locus by of an undifferentiated tubular collar and feather germ differential new barb ridge addition to each side of yielded the first feather, a hollow cylinder. Stage the follicle led to the growth of a closed pennaceous II—The origin of differentiated barb ridges resulted in feather with an asymmetrical vane resembling mod- a mature feather with a tuft of unbranched barbs and ern rectrices and remiges. Stage Vb—Division and a basal calamus emerging from a superficial sheath. lateral displacement of the new barb loci yielded op- Stage IIIa—The origin of helical displacement of barb posing, anteriorly and posteriorly oriented patterns of ridges and the new barb locus resulted in a pinnate helical displacement producing a main feather and an feather with an indeterminate number of unbranched afterfeather with a single calamus. The afterfeather barbs fused to a central rachis. Stage IIIb—The origin could have evolved at any time following Stage IIIb, of peripheral barbule plates within barb ridges yield- but likely occurred after Stage IV based on modern af- ed a feather with numerous branched barbs attached terfeather morphology. See Prum (1999) for details of to a basal calamus. There is insufficient information to additional stages in the evolution of feather diversity establish a sequence for Stage IIIa and Stage IIIb, but (Stages Vc–f). April 2003] Commentary 557

of feather development the two surfaces of a planar feather are not homologous with the two surfaces of a planar scale, and could not have evolved from them (Prum 1999, Prum and Brush 2002). Unfortunately, that fundamental fact was ignored by Heilmann (1926), who revived the elongate scale theory of feather evolution, and by the generations of ornithologists who sub- sequently advocated elongate scale hypotheses (Lowe 1935, Becker 1959, Parkes 1966, Maderson 1972, Regal 1975, Dyck 1985, Martin and Czerkas 2000), including two decades of publications by Feduccia (1980, 1985, 1993, 1996, 1999a, b). Elongate scale theories of feather evolution were falsifi ed on the basis of developmental evidence more than a century ago, and no proponent of the elongate scale theory has ever countered Davies’ (1889) fatal developmental FIG. 3. A schematic illustration of the helical growth of the primary branched structure of a pennaceous observations (Prum 1999, Prum and Brush 2002). feather with afterfeather from Lucas and Stettenheim Furthermore, no elongate scale model has ever (1972). Feathers are epidermal tubes that grow from presented a satisfactorily detailed hypothesis the base. Pennaceous feathers obtain their planar of the evolution of feather branched structure form only after emerging from the cylindrical feather (Prum and Brush 2002). Any theory of the origin sheath when growth is complete. The obverse (upper) of feathers should also explain the evolution of and reverse (lower) surfaces of a pennaceous feather how feathers grow, and elongate scale theories vane are created by the outer and inner surfaces, re- have entirely failed that test. spectively of the tubular feather germ. The surfaces of Elsewhere (Prum 2001, Prum and Brush a planar feather are not homologous with the dorsal (upper) and ventral(lower) surfaces of a planar scale, 2002), I have criticized the recent hypothesis which develop from the dorsal and ventral surfaces that the elongate scales of Longisquama are ho- of the initial scale outgrowth. Thus, the planar feather mologous with feathers (Jones et al. 2000). could not have evolved from an elongate planar scale Feduccia (2002) criticized my observations of (Davies 1889, Prum 1999, Prum and Brush 2002). Longisquam as cursory, but he neglected to mention that he has repeatedly published ob- Third, our molecular developmental experi- servations that are entirely in agreement with ments are not based on the theropod hypothesis mine (Prum 2001). For example, he wrote, “In (Harris et al. 2002). Rather, our data consist of 1982 I examined the specimen of Longisquama observations and experiments on the cellular in Moscow and could see no indication that molecular signaling mechanisms involved in the elongated scales were particularly feather- feather morphogenesis. Those data are entirely like” (Feduccia 1985:76). In 1999, he wrote, independent of, and entirely congruent with, “No doubt… the scales of Longisquama were the theropod origin of birds. not transmuted into feathers, but the specimen Feduccia stated that the scale-to-feather does show the tremendous experimentation model “conforms nicely to what we know about in feather-like scales in the basal archosaurs feather .” That is patently incor- before the advent of feathers” (Feduccia 1999b: rect. The dorsal and ventral surfaces of a scale 133). Somehow, he made a complete and rapid form from the dorsal and ventral surfaces of conversion from thinking that Longisquama was the fi rst primordial scale outgrowth, whereas a “bizarre and unique solution to the problem the obverse (outer) and reverse (under) sur- of gliding” (Feduccia 1999b: 95) to thinking faces of a pennaceous feather develop from the that Longisquama is the closest known relative outer and inner surfaces of the tubular feather of birds (Jones et al. 2000). germ, respectively (Fig. 3) (Davies 1889, Lucas Although Feduccia complimented our recent and Stettenheim 1972, Prum 1999). As Davies experimental research on feather development, (1889) fi rst pointed out, because of the topology he failed to grasp the consequences of our data 558 Commentary [Auk, Vol. 120

FIG 4. Congruence between patterns of expression a Sonic Hedghog (Shh) and Bone Morphogenetic 2 (Bmp2) molecular module during the evolution of a feather (above), and the developmental model of feather evolution (below) (Prum 1999, Harris et al. 2002). Shh and Bmp2 have distinct patterns of expression at four stage of feather growth (top, left to right): anterior–posterior polarized Shh/Bmp2 expression in the placode stage of feathers and scales; distal coexpression during development of the tubular feather germ; longitudinal Shh/Bmp2 expression in the folded marginal plate epithelium between barb ridges during the development of differentiated barbs (see cross-section of a barb ridge inset); and ventral bifurcation and dorsal cessation of Shh/ Bmp2 stripe expression during helical growth of a pennaceous vane. Each of those developmental evolution- ary novelties evolved by cooption, or evolutionary reutilization, of the primitive Shh/Bmp2 molecular module in a new context. The first, elongate tubular feather (Stage I) evolved from a primitive archosaurian scale by derived distal Shh–Bmp2 coexpression (Event 1). The first, branched plumulaceous feather (Stage II) evolved by the origin of derived longitudinal Shh–Bmp2 expression domains (Event 2) that created differentiated barbs from the tubular epithelium of the feather germ. A simple, pinnate pennceous feather (Stage IIIa) evolved by the controlled dorsal (d) cessation and ventral (v) bifurcation of the longitudinal Shh–Bmp2 expression domains (Event 3), producing helical growth of barb ridges, indeterminate barb number, a rachis, serial fusion of barbs to the rachis, and a planar vane. Subsequent events in the development and evolution of feathers—for example, origins and differentiation of barbules—will require additional mechanistic explanations. Abbreviations: c = central; d = dorsal, ph = peripheral, v = ventral.

(Harris et al. 2002). We demonstrated that feath- polarized expression of Shh and Bmp2 with the ers evolved through a series of cooptions— placodes of bird scales and alligator scales, but evolutionary reutilizations—of a plesiomorphic that all subsequent stages of feather develop- molecular developmental molecular module ment are derived and unique to feathers (Fig. (Fig. 4). The identifi ed elements of that mo- 4). Then the feather bud develops by distal co- lecular module consists of a pair of intercellular expression of Shh and Bmp2, creating the tubu- signaling genes Sonic Hedgehog (Shh) and Bone lar feather germ (Fig. 4, Event 1). Subsequently, Morphogenetic Protein 2 (Bmp2). Shh and Bmp2 barb ridges develop through longitudinal have conserved set of developmental interac- stripes in Shh and Bmp2 expression (Fig. 4, tions within the integument, like mechanical Event 2). Ultimately, the ventral new barb locus components of a machine. This molecular mod- and the rachis develop through the coordinated ule has been repeatedly recruited for controlled ventral bifurcation and dorsal cessation of Shh morphogenesis of novel structures during the and Bmp2 signaling stripes (Fig. 4, Event 3). evolution of feathers and feather complexity The molecular developmental data provide a (Fig. 4). We have shown that in the fi rst stage, transition series in the evolution of feathers and feather placodes share an anterior–posterior feather branched complexity that is based en- April 2003] Commentary 559 tirely on the molecular developmental experi- As Thomas Kuhn (1970:79) wrote in The ments (Fig. 4) (Harris et al. 2002). Compellingly, Structure of Scientifi c Revolutions, these independent molecular data are exactly congruent with predictions of the developmen- To reject one paradigm without simultane- tal model of the evolution of feathers which ously substituting another is to reject science was based on the classical feather development itself. That act refl ects not on the paradigm but literature (Fig. 2) (Prum 1999). Our fi ndings on the man. Inevitably, he will be seen by his demonstrate that feathers are homologous with colleagues as “the carpenter that blames his scales at the placode stage, but that the feather tools.” bud and all subsequent feather structures are evolutionary novelties that are not homolo- By offering no testable alternative to the gous with a scale or parts of a scale. Many of theropod origin of birds and maintaining that the molecular signaling systems involved in the origin of birds is potentially unsolvable, the initial development of scales and feathers Feduccia and other critics of the theropod hy- are shared between the two structures because pothesis of avian origins reject science itself. of the homology of their placodes. These ple- One-sided rejections of the theropod origin siomorphic similarities permit the experimental refl ect not on the hypothesis, but on intellectual manipulation of scale development, producing weaknesses of the critiques. the “transformation” of scale placodes into In my Perspectives essay, I wrote that, “it is feather placodes, as cited by Feduccia (2002). In time to end debate on the theropod origin of no way, however, do those experiments support birds, and to proceed to investigate all aspects the general homology of parts of feathers and of the biology of birds in light of their theropod scales, as required by the hypothesis that feath- origin.” In his response, Feduccia documents ers evolved from elongate scales. that the scientifi c debate is indeed over because The developmental model of the origin of current critics of the theropod origin of birds feathers (Prum 1999) has now been supported by are not doing science. The unrelenting prog- both paleontological (Prum and Brush 2002) and ress and success of the theropod hypothesis in molecular data (Harris et al. 2002). The develop- recent years is not the result of an overzealous mental theory of the origin of feathers, the new cladistic conspiracy, but the congruence of mul- Shh–Bmp2 data of feather development (Harris tiple lines of evidence from many workers to- et al. 2002), and the theropod hypothesis of the ward a coherent understanding of the origins of origin of birds provide the fi rst coherent under- birds, feathers, and now fl ight (Prum 2003). In standing of the origin and evolution of feathers. future decades, historians of science will doubt- less look back on this episode in ornithological CONCLUSION history as a classic example of the sociology In his commentary and previous publica- of science. Ornithologists should to let these tions, Feduccia has proposed a hypothesis of unworthy and unscientifi c arguments fade into avian origins that is untestably vague, inter- scientifi c history, and dedicate themselves to preted evidence inconsistently in favor of his the fascinating new scientifi c frontier of estab- hypothesis, rejected objective scientifi c methods lishing a thorough historical understanding the of reconstructing evolutionary history, changed origins of avian biology. the standards of evidence when new data are produced, and assumed the existence of con- ACKNOWLEDGMENTS vergence that has yet to be demonstrated (i.e. begged the question). Now, having accepted the I would like to thank R. Dahn, Matthew Harris, M. Robbins, R. Shafer-Landau, T. Peterson, and G. existence of feathered dromaeosaurs, Feduccia Wagner for suggestions and discussion. X. Xing and has contradicted decades of his own work by Z. Zhonghe kindly gave permission to reproduce hypothesizing that dromaeosaurs are actually their photo of Microraptor gui. fl ightless birds in order to maintain the same conclusion—that birds are not theropod dino- saurs. Feduccia’s rhetoric is beyond qualifying LITERASTURE CITED as the “most subjective and qualitative fi eld of biology.” My conclusion is that this is not sci- BECKER, R. 1959. Die Strukturanalyses der ence, but a rhethorical sham. Gefi ederfolgen von Megapodius freyc. reinw. 560 Commentary [Auk, Vol. 120

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