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Cross-Testing Adaptive Hypotheses: Phylogenetic Analysis and the Origin of Bird Flight1 KEVIN PADIAN2 Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley, California 94720-3140
SYNOPSIS. Adaptive scenarios in evolutionary biology have always been based on incremental improvements through a series of adaptive stages. But they have often been justified by appeal to assumptions of how natural selection must work or by appeal to optimality arguments or notions of evolutionary process. Cladistic methodology, though it cannot logically falsify hypotheses of process, provides hypotheses of evolutionary pattern independent of other considerations and so provides a useful test of consilience with genealogy. I illustrate the cross-test of hypotheses of the evolution of several functions and adaptations related to the origin of bird flight with independently derived phylogenetic analysis. Consilience does not support ideas that the close ancestors of birds were arboreal or evolved flight from the trees, nor that they were physiologically intermediate between typical reptiles and living birds, nor that feathers evolved for flight. Rather, the ancestors of birds were terrestrial, they were fast-growing, active animals, and the original functions of feathers were in insulation and coloration.
INTRODUCTION In 1965, Walter Bock published an important and influential paper that discussed how breakthroughs into new adaptive zones contributed to the formation of higher taxa. He illustrated this with an example of the evolution of bird flight, which is reproduced in Figure 1, and he contrasted two scenarios. In the first, birds evolve flight somehow in one fell swoop from a quadrupedal, ground-dwelling reptile. In the second, they pass through a series of stages that get them up on two legs, then climbing trees, jumping between branches and then between trees, then parachuting, gliding, and finally flapping. The first scenario, of course, can be disregarded as a straw man, because it has never been a serious contender. It would require a sudden transformation of forelimbs from a retractive, terrestrial, weight-bearing stroke to a depressive, protractive, aerial, thrust-generating stroke. The second scenario is of interest for two reasons. First, it 1 From the Symposium Beyond Reconstruction: Using Phylogenies to Test Hypotheses About Vertebrate Evolution presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2000, at Atlanta, Georgia. 2 E-mail: kpadian@socrates.berkeley.edu
embodies several principles of the Modern Synthesis of evolution: complex adaptations should evolve piece by piece and gradually, and every stage along the way to the eventual endpoint of the adaptive process should themselves be adaptive. And second, no real animals are included in this scenario. Is it important that no real animals are presented in a scenario for the evolution of the central adaptation of a major group? Perhaps not in this case, because at the time Bock wrote, the origin of birds was, as they say, shrouded in mystery. It is perhaps more interesting that Bock’s first, ‘‘ground-dwelling’’ scenario was not more creative. Even in the ‘‘cursorial’’ or ground-based models of the origin of flight proposed in the 1880s, quadrupedal reptiles got up on two legs, ran along the ground, and used their outstretched arms (variously feathered, depending on the author) to gain lift and eventually thrust (reviews in Ostrom, 1974; Padian, 1985, 1995; Witmer, 1991). But again, no actual animals were involved in this scenario either. Since the early 1970s, three principal advances have changed the way we look at this question. The first occurred in 1973, when John Ostrom proposed that birds
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FIG. 1. A classic dichotomy of macroevolutionary analysis, from Bock (1965). Scenario ‘‘A,’’ however, does not realistically represent most models of groundbased flight origins proposed since the 1880s.
evolved from small carnivorous dinosaurs. There were simultaneous competing hypotheses that birds evolved either from crocodiles (e.g., Walker, 1972) or from unspecified basal archosaurs (‘‘thecodontians’’; e.g., Tarsitano and Hecht, 1980). But these hypotheses gradually went by the wayside because the proposed similarities were shown to be convergences, or else no specific taxa beyond a cloud of vague or imaginary primitive forms were proposed for testing (see Gauthier and Padian, 1985; Gauthier, 1986; Witmer, 1991; Dingus and Rowe, 1997; Padian and Chiappe, 1998a, b). The second advance was the rise of cladistics, which made phylogenetic hypotheses explicit. Workers had successively less patience with claims of bird ancestry from unspecified basal archosaurs, ‘‘avimorph thecodonts,’’ and other phantasms. Every time a cladistic analysis was performed, birds wound up evolving from small carnivorous theropod dinosaurs (e.g., Gauthier, 1986; Holtz, 1994; Forster et al., 1998; Makovicky and Sues, 1998; Sereno, 1997; Xu et al., 1999a, b, to name only a few examples). No dissident from the dinosaurbird hypothesis has published a rigorous cladogram, and some explicitly denounce phylogenetic analysis (e.g., Feduccia, 1996; Dodson, 2000), without proposing a testable method in its place. The third advance was the realization that the classic arboreal (or ‘‘trees down’’) and cursorial (or ‘‘ground up’’) dichotomy is a false one. The central problem of the
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origin of bird flight is the evolution of the flight stroke, which generates thrust. Rayner (1985a, b, 1991, 2001) focused on the importance of this problem in aerodynamic terms, and Padian (1982, 1985, 1987, 1995, 2001a) discussed it in functional and evolutionary contexts. Strictly speaking, it does not matter whether this stroke evolves in the trees or on the ground, and there is evidence that it can happen in both milieus (e.g., Gauthier and Padian, 1985; Norberg, 1985; Dingus and Rowe, 1998; Padian and Chiappe, 1998a, b; Burgers and Chiappe, 1999; Dial, 2001). We are not likely ever to settle the classic version of the question, because we will not find extinct birds fossilized as they leap from trees or jump up from the ground in mid-flight. REFORMULATING THE PROBLEM The rise of cladistics has reversed a traditional way of thinking about major features of evolution. Not long ago, decisions about phylogenetic relationships were often based on the behavioral, ecological, or functional plausibility that one taxon could have evolved from the other. This judgment depended on the interpretation of structures and features in each taxon and suppositions about how evolutionary patterns would be expected to occur, given assumptions about how evolutionary processes should work. Taxon A could not have evolved from Taxon B because B was too specialized, or too large, or lived in a different environment, or used its structures for a different purpose. Cladistics took the focus off direct ancestry and put it on shared ancestry, to be assessed strictly on the possession of synapomorphies. It also removed hypotheses of process and function from assessments of relationship, which were now based solely on the analysis of pattern. Instead, in the cladistically influenced comparative method developed in the past three decades, hypotheses about the evolution of function, behavior, or ecology are tested by cladograms (e.g., Eldredge and Cracraft, 1980; Brooks and McLennan, 1991; Lauder et al., 1995). The word ‘‘test’’ in this context has a complex meaning that invites careful consideration. In general, I use it to describe the comparisons of inde-
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pendent outcomes in search of inductive consilience. That is, we compare the results of independent lines of investigation to see if they are similar enough to converge on the same conclusion. Strictly speaking, cladograms are hypotheses of relationship; they cannot falsify other kinds of hypotheses. Yet in practice, they sometimes seem to be given inordinate weight. For example, Perle et al. (1993), in describing Mononykus, found synapomorphies that placed it within Aves, just a step closer to living birds than Archaeopteryx is. Yet the bizarre Mononykus had tiny forelimbs with a single digit and was obviously flightless. Inasmuch as the outgroups to Archaeopteryx and the other birds were also flightless, Perle et al. concluded that it was ‘‘equally parsimonious’’ to decide that Mononykus was secondarily flightless or to decide that flight had evolved twice in birds (once in Archaeopteryx, and once in the birds after Mononykus). In theory, this may be true, providing we keep clear what our theoretical justification is. But it may violate the philosophy of parsimony. If one only considers the shortest number of steps on a tree, then by the criteria of methodological parsimony it would be equally parsimonious to choose either hypothesis to pursue first for further testing (Johnson, 1982). However, on the shakier grounds of ontological parsimony, when the two hypotheses are regarded as equally probable, one makes assumptions about how ‘‘easy’’ or ‘‘likely’’ it is to evolve flight twice—a proposition that a cladogram alone cannot determine, because it is merely a simple statement about the distribution of synapomorphies among a set of taxa. Of course, no hypotheses about the origin of flight have been falsified, and so all must be considered possible to some degree, if not equally plausible. However, the results of a single cladogram are overweighted if they are allowed to arbitrate or preclude given functional scenarios—just as if hypotheses about how certain processes ‘‘must’’ work in evolution are allowed to preclude certain phylogenetic hypotheses (such as the impossibility of the evolution of birds from dinosaurs on the basis of functional-ecological presumptions: Bock,
1986; Feduccia, 1996). Hypotheses about the evolution of functions and behaviors must be based on different evidence than the phylogenetic hypotheses, because otherwise they will have no intellectual content (Padian, 1982, 1995). A phylogenetic analysis is an important component of the formation of any evolutionary theory. Some cladograms have pointed the way to further analysis of process-based evolutionary hypotheses. On the other hand, preliminary cladograms have often been abandoned in favor of more rigorous analyses that included more taxa and characters. Whewell (1840) called this approach consilience, or how consistent independent lines of evidence are with each other. Quite often, a given cladogram is inconsistent with a result from biostratigraphy or biogeography, which like cladograms are historical patterns. For example, a commonly accepted phylogenetic hypothesis is that ceratopsian and pachycephalosaurian dinosaurs are sister taxa that diverged from other ornithischian dinosaurs sometime in the Triassic Period (Sereno, 1986). Yet fossils of neither group have so far been found until the Early Cretaceous, some 100 million years later, by which time all other dinosaurian groups thought to have diverged from them are well represented in the fossil record. An alternate view, that ceratopsians and pachycephalosaurs diverged from ornithopod dinosaurs in the Late Jurassic (Norman, 1984), is more consistent with the preserved biostratigraphic evidence. Here, a pattern (in this case, of biostratigraphy) tests another pattern (of relationship), not a hypothesis of process. But still no hypothesis is falsified. The question is one of consilience. It may be argued that phylogenetic and functional hypotheses cannot be compared on an equal footing, because characters used in phylogeny are actually preserved, whereas function must be a second-order inference. This view is completely reasonable, even though caveats must be attached. First, characters must be interpreted, their states parsed out, and their polarities assessed; they are not objective entities. Second, quite often there are several plausible competing cladograms with very different
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FIG. 2. Cladogram of theropod dinosaurs, based on analyses in Gauthier (1986), Holtz (1994), Forster et al. (1998), Makovicky and Sues (1998) Sereno (1997), Xu et al. (1999a, b, 2000), and other sources. Some features classically related to the origin of birds or to flight are superimposed.
implications for functional and physiological evolution: current hypotheses about the origins of turtles, snakes, and whales are useful examples. Third, biostratigraphic data represent a set of information, ordered by evolution through time, and internally testable, that form patterns—just as phylogenetic and functional data do. I would agree, however, that if a phylogeny is well supported, it offers difficult obstacles and constraints to hypotheses of functional or behavioral evolution that are inconsistent with it. FUNCTIONAL PREDICTIONS AND PHYLOGENETIC TESTS It is possible that hypotheses of pattern, such as cladograms, can test hypotheses of process, if the latter hypotheses have predictions that can be tested by the comparison of expected patterns. As noted above, the ‘‘cursorial/arboreal’’ dichotomy of competing scenarios that purport to explain the origin of flight is largely untestable and unproductive. Still, it can be used instructively to show how predictions of evolutionary hypotheses can be tested. The traditional arboreal scenario (Fig. 1) would predict that features functionally related to climbing, jumping, parachuting, and gliding would be found successively in
the ancestry of birds, if such features or their structural correlates could be preserved at all. Because there is no alternative phylogenetic analysis to the consensus cladogram presented in Figure 2, the latter represents a de facto phylogeny by which to test hypotheses of the evolution of flight based on predictions of mechanical evolution. There are, to be sure, minor differences among current cladograms of the immediate relatives of birds, principally because there are multiple convergences among some fine details of features (Holtz, 1994; Forster et al., 1998; Makovicky and Sues, 1998; Sereno, 1997; Xu et al., 1999a, b, 2000). However, the details make no real difference to the mechanical evolution of features crucial to flight (Padian, 1998). The objective is to elucidate the predictions of alternate functional models and see if the character-state changes of independently derived phylogenetic analyses are consilient with them. If the traditional arboreal scenario were a good predictor of the phylogenetic distribution of flight-related characters (Fig. 1), we would expect to see structural correlates of climbing, gliding, and finally flapping appear in that order. Chatterjee (1997) has provided the most detailed argument for a climbing ability of protobirds, but it was
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not based on a true functional analysis of the animals antecedent to birds. The climbing scenario seems to be contradicted by Gishlick (2001), who shows that Deinonychus, a typical member of the immediate sister-group to birds (Fig. 2), had a forelimb motion that was considerably restricted and quite different from anything like climbing. Unless closer relatives of birds with a different movement can be found—and so far no analysis of Archaeopteryx shows that it could climb—this function cannot be assumed, even if it cannot be excluded. (Many small and some large tetrapods with no obvious arboreal features can get into trees.) Microraptor, a small and evidently basal dromaeosaur, is said to have arboreal features (Xu et al., 2000), but this was based only on foot claw curvature, which is not as good a predictor of habitat as phalangeal proportions are (Hopson and Chiappe, 1998). Yalden (1985, 1997) argued that the claw morphology and skeletal proportions of Archaeopteryx were consistent with those of some scansorial mammals. But both types of features were already present in larger non-avian theropods that neither climbed nor flew, and the claw and foot proportions of Archaeopteryx do not argue for arboreality any more than for grounddwelling (Hopson and Chiappe, 1998). These features were inherited from more basal theropods and cannot be viewed as adaptations for arboreality or flight. Gliding is more complex to analyze because many small tetrapods can slow descent merely by flattening their bodies and expanding their surface area to enhance lift and drag (Moffett, 2000). As Padian (1985) discussed, few definitive skeletal features separate gliders from their non-gliding relatives. However, if we look at birds, we do not find evidence of an airfoil between fore and hind limbs that characterizes most gliders today. (To my knowledge, the rib-membrane present in Draco today has never been seriously proposed as a property of protobirds.) In sum, the structural predictions of the arboreal scenario are only poorly supported by the phylogenetic pattern. The traditional cursorial predator hypothesis suggests that the ancestors of birds were active ground-dwelling animals that
used their arms in predation. The predatory motion eventually was exapted to a flight stroke (Gauthier and Padian, 1985). The evolution of birds (Fig. 2) shows that forelimb length increased, and that this stroke (Gauthier and Padian, 1985; Gishlick, 2001) was very similar to the flight stroke of birds in being a down-and-forward, upand-backward motion. Only birds and other maniraptorans can flex their wrists sideways, rotating as they do so (Ostrom, 1997), to produce a movement that rushes air over the wings and creates lift and thrust (Rayner, 1985a, b). In sum, the structural predictions of the cursorial scenario are completely consistent with the phylogenetic pattern. The cursorial scenario also does a better job of focusing the attention away from the ecological setting of the evolution of flight and toward the evolution of the flight stroke, which is the central problem of flight, as noted above. This stroke must generate thrust as well as lift; it requires an airfoil with aerodynamic integrity. To study the evolution of this adaptation requires identification of structures with functional significance for the flight stroke. The phylogeny in Figure 2 shows that a number of features conventionally thought to have evolved ‘‘for’’ or in connection with flight, such as the thin-walled bones, the sternum, the furcula, the elongated forelimb elements, and so on, were already present in the ancestors of birds, presumably connected with other functions or behaviors. In the past few years, another line of evidence has emerged that may eventually clinch the argument in all but the most diehard of skeptics: namely, the presence of feathers and related integumentary features in the theropod relatives of birds. TELLING THE TREE Given that a cursorial origin of flight appears more in accordance with the cladogram presented in Figure 2, can other lines of evidence be adduced to test consilience (Padian, 1987, 1995)? I briefly consider here two independent lines of evidence with hypotheses that can help test how much ‘‘sense’’ the cladogram makes, and be tested themselves by the hypothesis that this
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FIG. 3. Cladogram of feathered dinosaurs with features of the integument superimposed. The pattern suggests that filamentous structures, probably homologous to true feathers (see Padian et al., 2001), first appeared at least in basal coelurosaurs, and several kinds of true feathers shortly thereafter. These filamentous structures have not so far been found in true birds. For explanation see text.
phylogeny is somewhat accurate. I discuss the evolution of feathers, and the evolution of small size and growth strategies in basal birds. THE EVOLUTION OF FEATHERS Since 1996, the discovery of coelurosaurian dinosaurs (the closest known taxon to birds) with remnants of several kinds of integumentary structures, including feathers, has revolutionized our thinking about the origin of feathers (Chen et al., 1998; Ji et al., 1998; Padian et al., 2001). It also provided another line of evidence that birds evolved from these theropods. The animals in question are all from the Early Cretaceous Liaoning deposits of China. Those with filamentous integumentary structures include the compsognathid Sinosauropteryx (Chen et al., 1998), the therizinosauroid Beipiaosaurus (Xu et al., 1999a), the maniraptoran Sinornithosaurus (Xu et al., 1999b), and the alvarezsaurid Shuvuuia (Schweitzer et al., 1999) (which unlike the other taxa is found in the Late Cretaceous of Mongolia). The oviraptorosaur Caudipteryx and its apparently close relative Protarchaeopteryx both have such filaments, but they also have several kinds of true feathers on their hands, tails, and bodies (Ji et al., 1998; Padian et al., 2001). Figure 3
shows the phylogenetic distribution of these structures. The first question is how the structures of feathers evolved, and this is still not entirely clear. The filaments of Sinosauropteryx, Beipiaosaurus, and Sinornithosaurus are thick and coarse. In Caudipteryx and Protarchaeopteryx the smaller, isolated plumulaceous feathers may represent such filaments gathered into tufts. The shafts of these feathers may have been formed by the consolidation of individual filaments. The shafts are approximately the same length as the terminal filaments, which apparently do not branch and do not have central shafts (Padian et al., 2001). Shafts and vanes are present in the feathers of Caudipteryx and Protarchaeopteryx, but no direct evidence of the shafts remains. The vanes have parallel barbs, which suggests the presence of barbules. However, in these taxa the feathers are far too short for flight, as are the forelimbs themselves, given the size of the animals. If feathers did not evolve directly for flight, why did they evolve? The integumentary structures of Sinosauropteryx would have had an insulatory function simply because they are so long and densely distributed all over the body. Feathers, like fur, may have evolved first as insulatory
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structures in neonates but were maintained and elaborated in adults for different purposes. But why would an insulatory function, in the form of elaborate feathers, be more useful in adults than in neonates? Integumentary structures can retain heat or help to shed it. Behavioral thermoregulatory strategies may have preceded the evolution of such integumentary structures, which in turn allowed further behavioral and ecological possibilities. Several examples are now known of oviraptorids sitting on their nests as birds do today, using their forelimbs to cover their eggs (Hopp and Orsen, 2001; Clark et al., 1999). The distribution of feathering along the arms in Caudipteryx and Protarchaeopteryx suggests that flight was impossible. It also suggests that an insulatory function may have been more important in adults for the purpose of the young than it was for either the adults or young in their own thermoregulation (Padian et al., 2001). THE EVOLUTION OF SMALL SIZE IN BIRDS When birds became small, having evolved from larger coelurosaurian dinosaurs, how did they change their growth strategy? The microscopic tissues of bones vary greatly among organisms, and are more closely tied to developmental factors than any other (Amprino, 1947; Castanet et al., 1993; Ricqle`s et al., 2001), though phylogenetic, environmental, and mechanical factors also play important roles. These tissue types have characteristic ranges of depositional rates across living vertebrates, so it appears reasonable to presume that the same tissues in extinct animals would have had comparable rates of growth and deposition. Given this working hypothesis, the comparative histology of bone tissues in basal birds and nonavian dinosaurs can be usefully placed in phylogenetic perspective to test hypotheses about what happened in the early evolution of avian growth strategies. Armand de Ricqle`s, John R. Horner, and I have been investigating this question with respect to extinct theropod dinosaurs and both extinct and extant birds (see Ricqle`s et al., 2001, and references therein). Nonavian theropods have long bone cortices that are
primarily composed of fibrolamellar bone deposited in regular laminae with numerous vascular canals that run both longitudinally and circumferentially, and anastomose frequently in all directions, through most of their growth. This tissue is very much like the tissue that predominates through most of the ontogeny of larger birds today, and it reflects rapid growth, perhaps owing to a faster-growing lamellar component (Rensberger and Watabe, 2000). Some basal birds, like some small birds today, have cortices that are more compact and poorly vascularized, and the two bones sampled from enantiornithines (Chinsamy et al., 1995) were particularly deficient in these respects. In their poor vascularization and predominance of longitudinal vascular canals, they resemble the tissues of more slowly growing reptiles, which prompted the hypothesis that these early birds may not have been fully endothermic (Chinsamy et al., 1995). Later Cretaceous birds show more fast-growing tissue types, which suggested that they may have finally been approaching the physiological levels of extant birds (Chinsamy et al., 1998). Putting these and other observations in a phylogenetic and ontogenetic context (Fig. 4), our results suggest a different possibility (Ricqle`s et al., 2001). The bone tissues of nonavian theropods ostensibly reflect faster growth rates than those of basal birds, as do those of living birds. If a physiological interpretation is directly tied to tissue types, then one should accept that nonavian theropods were endothermic, but basal birds were not; however, later birds, including extant forms, would have to have reversed this pattern and become endothermic again. Instead, we suggest, these tissue types reflect changes in growth rates. The extended phase of deposition of well vascularized fibrolamellar bone reflects fast growth and allowed dinosaurs to reach the large sizes that they did. This is consistent with the observation that growth rates are higher in taxa of larger adult size than in those with smaller adult sizes (Case, 1978). To reach the smaller adult size of birds, their dinosaurian ancestors apparently lowered the growth rates in some or all ontogenetic phases, and also may have truncated the
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FIG. 4. Cladogram of theropod dinosaurs, including birds, with histological features of the bone tissues and the growth patterns they reflect superimposed on the phylogeny. Dinosaurs in general have bone tissues that suggest that they grew very quickly, and this growth rate was reduced in the first birds as they achieved smaller adult size; growth rates increased in the lineage leading to extant birds, enabling them to reach their smaller size faster. For explanation see text; details in Ricqle`s et al. (2001).
time it took to reach adult size. Consequently, their adult size was much smaller than in their nonavian relatives, with the exception of Microraptor (Xu et al., 2000). This hypothesis may also explain why the skeletal specimens of Archaeopteryx, which follow a single allometric trajectory, vary so much in size (Houck et al., 1990): Because basal birds grew more slowly than the 4–12 wk taken by most living birds to reach adult size, it may have been more likely that some would be preserved in the fossil record at less than adult size. CONCLUSION For two decades, works such as Eldredge and Cracraft (1980), Brooks and McLennan (1991), Rose and Lauder (1996), and Harvey and Pagel (1991) have provided examples of the use of phylogeny as an important part of consilience to be applied to evolutionary questions. These methods are further supported by most journals in the field of comparative biology (sensu lato). It is mystifying to find that some evolutionary biologists, including so many involved in the SICB symposium on ‘‘The Evolutionary Origin of Feathers’’ (American Zoologist 40 [4], 2000), continue to ignore phylogenetic information and methods in presenting their hypotheses of the evolution of structure, function, behavior, and physiology. Increasingly, such hypotheses are given less and less credibility by the community
at large because they are not framed phylogenetically (Padian, 2001b). Cladograms are not the arbiters of functional hypotheses, which must be developed independent of them (Padian, 1982, 1995). However, any hypothesis about evolutionary processes eventually must be measured against a well corroborated phylogenetic hypothesis (if one is recognized), because only phylogenetic hypotheses assess the actual pattern of evolution. It may always be claimed that not everyone accepts a given phylogeny, but unanimity is not required or assessed in science. Phylogenies must be tested continually, too. No method or single line of evidence can be assigned primacy of explanation, because evolutionary biology is an inductive science. However, by constant testing, revision, and cross-comparison of hypotheses derived from independent lines of evidence, evolutionary biologists can ensure that the science remains vigorous and objective. ACKNOWLEDGMENTS I thank Don Swiderski for the invitation to participate in the symposium, and the SICB and the Committee on Research at the University of California, Berkeley for support of travel. I also thank Steve Gatesy, John Rensberger, John Hutchinson, and Jim Parham for reviews of the manuscript, and Jack Horner, Armand de Ricqle`s, Ji Qiang, Ji Shu’an, Philip Currie, Richard Prum,
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