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Copyrighted Material 1 Theropod Diversity and the Refinement of Avian Characteristics PETER J. MAKOVICKY AND LINDSAY E. ZANNO Field Museum, Chicago, USA Bird origins have been debated ever since Darwin biologists such as Cope favored an evolutionary published his “Origin of Species,” and was subse- relationship between birds and ornithopod dino- quently challenged on the topic by Sir Richard saurs such as hadrosaurs, based again on a three- Owen, who pointed out the lack of transitional toed foot and a retroverted pubic shaft. While a fossil forms in the evolution of the highly derived variety of ancestors or sister taxa were proposed for avian body plan. Indeed, Owen likely carefully birds, a broad consensus that they were related to selected birds to make his point due to their dinosaurs prevailed until the publication of the many unique traits and physiological features English edition of Heilmann’s (1926) “Origin of such as flight, feathers, bipedality, and a remark- Birds.” Heilmann’s book presented a detailed able respiratory system in which the lungs are study of neontological, embryological, and fossil connected to and ventilated by a complex system evidence, all of which pointed to a theropod of air sacs that pneumatize the skeleton. Within ancestry for birds. Nevertheless, based on the two years of this debate, the discovery of the first prevailing assumption of the time that dinosaurs specimens of Archaeopteryx provided conclusive ancestors had lost their clavicles, their reappear- evidence of avian evolution in the fossil record and ance in birds would violate Dollo’s (1893) law of became the focal point for research and delibera- irreversibility. Heilmann therefore concluded tion on the topic for more than a century. While that the similarities between birds and theropods the fossils of Archaeopteryx provided incontro- were due to convergence, and that birds were vertible evidence for a reptilian origin for birds, derived from more basal archosaurs that still opinions varied as to which group of reptiles birds retain clavicles. may have originated from. Due to the thoroughness of his book, Following the discovery of the small nonavian Heilmann’s (1926) hypothesis held sway for the theropod Compsognathus in the same limestone next four decades until the discovery and descrip- deposits as Archaeopteryx, Huxley (1868) pre- tion of the mid-sized dromaeosaurid theropod sciently proposed an evolutionary relationships Deinonychus by Ostrom (1969). Ostrom’s detailed between birds and nonavianCOPYRIGHTED theropods based on study MATERIAL of the skeletal anatomy of Deinonychus led shared traits such as three principal, weight- him to recognize derived characters shared bearing toes in the foot (confirmed by foot-prints), between it and the basal bird Archaeopteryx a tall ascending process of the astragalus, and (Ostrom, 1976), and to the discovery of a misiden- hollow bones. Other contemporary evolutionary tified specimen of Archaeopteryx (Ostrom, 1970). Living Dinosaurs: The Evolutionary History of Modern Birds, First Edition. Edited by Gareth Dyke and Gary Kaiser. Ó 2011 John Wiley & Sons, Ltd. Published 2011 by John Wiley & Sons, Ltd. 10 PETER J. MAKOVICKY AND LINDSAY E. ZANNO Among the new traits that Ostrom mustered A ROADMAP TO THE DINOSAURIAN to revive a theropod ancestry for birds are the HERITAGE OF BIRDS presence of a half-moon-shaped wrist bone that allows the hand to adduct against the forearm as in Despite their radically different body plans, the wing-folding mechanism of living birds, and birds inherited a mosaic of anatomical traits a three-fingered hand with characteristic propor- from various stages of vertebrate history. A tions between the three metacarpals and phalan- host of discoveries over the past five decades ges. Following Ostrom’s work, progressively more provide a detailed road map to how the highly evidence has been amassed to support this hypoth- specialized avian anatomy was assembled over esis of avian origins, as a plethora of new fossil the evolutionary lineage leading to birds and discoveries continue to blur the morphological demonstrates that many of the traits that are distinction between birds and their closest thero- considered uniquely avian among extant pod relatives. amniotes actually arose before the origin of Over the past three decades, widespread adop- birds themselves. While most of our understand- tion of cladistic methodology for establishing ing of where birds fit into the tree of life comes and testing proposed evolutionary relationships fromstudyofhardtissues,dramaticnewdis- has provided the conceptual framework for deci- coveries in the past decade and a half are pro- phering the origin and evolutionary history of viding unprecedented insights on the evolution birds. Gauthier (1986) was the first to apply an of soft tissue systems (Schweitzer et al., 1999; explicit cladistic parsimony analysis of theropod Xu et al., 2001) aspects of physiology (Varricchio relationships to the question of bird origins. In et al., 2002; Varricchio & Jackson, 2004; doing so, he provided the first rigorous test of the Organ et al., 2007), and even behavior (Norell hypothesis of theropod ancestry and set the stage et al., 1995; Varricchio et al., 1997; Xu & Norell, for evaluating the evolutionary history of avian 2005). anatomy, physiology, and behavior in a quantita- That birds are archosaurs and the closest liv- tive framework. Subsequent decades have seen ing relatives to crocodilians has long been a remarkable surge in the discovery of new ther- inferred from shared derived traits such as a opods, including fossil stem birds, with each dis- four-chambered heart and thecodont dentition. covery spawning novel systematic analyses (for Virtually all birds possess an external mandibu- reviews see Weishampel et al., 2004; Norell & lar fenestra, a synapomorphy of Archosauria Xu, 2005; Benton, 2008) and further supporting (Benton, 1990) and fossil avians also possess an the hypothesis that birds are theropod dinosaurs. antorbital fenestra (Figure 1.1), also considered To date, profound advances have been made in a hallmark of this clade, although in extant teasing out the evolution of the avian body plan as birds the latter opening is lost or merged with well as correlated physiological features and life the external nares through expansion of the history parameters of modern birds. Likewise, premaxillae and concomitant reduction of our knowledge of these traits in modern birds other preorbital bones. Phylogenetic analyses and their anatomical correlates has been used to have identified numerous derived traits shared yield insight into the biology of nonavian theropod by birds and various hierarchically arranged dinosaurs and to infer whether particular avian subsets of archosaur diversity (Figure 1.1). A traits originated before or after the origin of the comprehensive review detailing all of these char- avian lineage itself. Here we provide a general acters is beyond the scope of this chapter, so here overview of the stepwise acquisition of the we concentrate on a select subset of traits and avian body-plan throughout the theropod family evolutionary branching points that are most crit- tree and discuss how the physiology of modern ical to understanding the evolution of the unique birds is being used to reconstruct aspects of dino- avian body plan and its derived physiological and saur biology. functional correlates. Theropod Diversity and the Refinement of Avian Characteristics 11 Fig. 1.1 Guide to avian evolutionary history based on a simplified evolutionary tree of Archosauria. Key traits in avian evolution are mapped onto the cladogram with their corresponding position indicated on the skeleton of Archaeop- teryx. Note how traits are distributed throughout the skeleton revealing the mosaic assembly of avian anatomy throughout ornithodiran evolution. See text for more detailed discussion of individual traits. Archaeopteryx recon- struction by M. Donnelly. 12 PETER J. MAKOVICKY AND LINDSAY E. ZANNO The deepest division among archosaurs is acetabula (Sereno & Arcucci, 1993) reveal that the between the lineages leading to the extant clades acquisition of a fully open acetabulum occurred in Crocodylia and Aves. Each of these branches also a gradual fashion spanning several branching subtends numerous fossil clades, which were points at the root of the dinosaurian evolutionary dominant faunal elements during the Mesozoic. tree (Figure 1.1). Counterintuitively, birds fall The avian total group (¼ extant plus extinct within the Saurischia, or “lizard-hipped” branch diversity after the split from the lineage leading of dinosaur diversity, rather than the Ornithischia, to Crocodylia) is known as Ornithodira and the “bird-hipped” branch. Saurischians are united is characterized principally by the possession of by their possession of hyposphen–hypantrum a mesotarsal ankle joint (Figure 1.1), in which accessory articulations between the neural arches the articulation between the foot and crus occurs of the trunk vertebrae, which are also marked by between the proximal and distal tarsals and lateral excavations on their neural arches presum- approximates a roller joint, restricting foot ably housing diverticula of the respiratory system. motions to fore–aft swinging without a rota- Hypantrum–hyposphen articulations were lost in tional component. Ornithodirans are also char- a later stage of bird evolution, but some fossil birds acterized by having a clearly defined femoral such as Patagopteryx reveal that this trait was head that
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