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Corresponding author. Email: Kevin Middleton@brown.edu ADDITIONAL KEY WORDS:Aves bipedalism Dinosauria disparity ight limb morphology locomotion morphospace Theropoda wing. CONTENTS Received August 1998; accepted for publication December 1998 2000 The Linnean Society of London doi:10.1006/zjls.1998.0193, available online at http://www.idealibrary.com on Zoological Journal of the Linnean Society (2000), 128: 149187. With 8 gures K. M. MIDDLETON AND S. M. GATESY 150 INTRODUCTION

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  • Zoological Journal of the Linnean Society (2000), 128: 149187. With 8 figures

    doi:10.1006/zjls.1998.0193, available online at http://www.idealibrary.com on

    Theropod forelimb design and evolution

    KEVIN M. MIDDLETON* AND STEPHEN M. GATESY

    Department of Ecology and Evolutionary Biology, Brown University, Providence,Rhode Island 02912, U.S.A.

    Received August 1998; accepted for publication December 1998

    We examined the relationship between forelimb design and function across the 230-million-year history of theropod evolution. Forelimb disparity was assessed by plotting the relativecontributions of the three main limb elements on a ternary diagram. Theropods were dividedinto five functional groups: predatory, reduced, flying, wing-propelled diving, and flightless.Forelimbs which maintained their primitive function, predation, are similarly proportioned,but non-avian theropods with highly reduced forelimbs have relatively longer humeri. Despitethe dramatically diVerent forces imparted by the evolution of flight, forelimb proportions ofbasal birds are only slightly diVerent from those of their non-avian relatives. An increase indisparity accompanied the subsequent radiation of birds. Each transition to flightlessness hasbeen accompanied by an increase in relative humeral length, which results from relativelyshort distal limb elements. We introduce theoretical predictions based on five biomechanicaland developmental factors that may have influenced the evolution of theropod limb pro-portions.

    2000 The Linnean Society of London

    ADDITIONAL KEY WORDS:Aves bipedalism Dinosauria disparity flight limbmorphology locomotion morphospace Theropoda wing.

    CONTENTS

    Introduction . . . . . . . . . . . . . . . . . . . . . . . 150Material and methods . . . . . . . . . . . . . . . . . . . 151

    Systematics and terminology . . . . . . . . . . . . . . . . 151Data collection . . . . . . . . . . . . . . . . . . . . 152Analysis: ternary diagrams . . . . . . . . . . . . . . . . 152Disparity index . . . . . . . . . . . . . . . . . . . . 152Functional groups . . . . . . . . . . . . . . . . . . . 154

    Results . . . . . . . . . . . . . . . . . . . . . . . . 154All theropods . . . . . . . . . . . . . . . . . . . . . 154Predatory . . . . . . . . . . . . . . . . . . . . . . 154Reduced . . . . . . . . . . . . . . . . . . . . . . 155Flying . . . . . . . . . . . . . . . . . . . . . . . 155Wing-propelled diving . . . . . . . . . . . . . . . . . . 156Flightless . . . . . . . . . . . . . . . . . . . . . . 158

    Discussion . . . . . . . . . . . . . . . . . . . . . . . 158Predatory . . . . . . . . . . . . . . . . . . . . . . 160

    *Corresponding author. Email: Kevin Middleton@brown.edu

    14900244082/00/020149+39 $35.00/0 2000 The Linnean Society of London

  • K. M. MIDDLETON AND S. M. GATESY150

    Reduced . . . . . . . . . . . . . . . . . . . . . . 160Origin of flight . . . . . . . . . . . . . . . . . . . . 162Flying birds . . . . . . . . . . . . . . . . . . . . . 162Wing-propelled diving . . . . . . . . . . . . . . . . . . 162Flightless . . . . . . . . . . . . . . . . . . . . . . 163Limb proportion theory . . . . . . . . . . . . . . . . . 163

    Conclusions and prospects . . . . . . . . . . . . . . . . . . 167Acknowledgements . . . . . . . . . . . . . . . . . . . . 167References . . . . . . . . . . . . . . . . . . . . . . . 167Appendix 1 . . . . . . . . . . . . . . . . . . . . . . . 172Appendix 2 . . . . . . . . . . . . . . . . . . . . . . . 173Appendix 3 . . . . . . . . . . . . . . . . . . . . . . . 184

    INTRODUCTION

    One of the fundamental features of any limbs design is the relative proportionsof its skeletal components. These proportions are often expressed as the ratio of twobone lengths, such as the femorotibial and humeroradial indices (Howell, 1965).Such ratios are thought to have functional significance for limb use because theyreflect the basic layout of an appendages compound lever system. Most frequently,proportions have been employed to identify and categorize mammalian limbsspecialized for running, weight support, or digging (Gregory, 1912; Osborn, 1929;Smith & Savage, 1956; Garland & Janis, 1993; Gebo & Rose, 1993; Carrano, 1997).Proportions have also been invoked as indicators of cursoriality in dinosaurs (e.g.Osborn, 1916; Ostrom, 1976a; Coombs, 1978; Colbert, 1989; Holtz, 1995a; Serenoet al., 1996). The majority of work to date has focused on limbs used for terrestriallocomotion. Such limbs bear loads by transmitting muscular, gravitational, andinertial forces to the substrate, and thus lend themselves to hypotheses based onlever mechanisms.

    Comparatively little is known about limbs that are not loaded in this manner.Forelimbs used during flight, prey capture, or food manipulation likely experiencemechanical forces quite diVerent from those used exclusively during terrestriallocomotion but with a few exceptions (Mattison & GiYn, 1989; Mattison, 1993;Christiansen, 1997), remain relatively unexplored. Theoretical predictions are few,and many questions remain unanswered. For example, how well does the relativesize of skeletal elements reflect limb function? How should a predatory forelimb beconstructed, and how might this arrangement diVer from that of a wing? Are limbproportions informative about the evolutionary origin of flight and secondary lossof volant function? Do the demands of flight impose strong constraints on wingdesign?

    Theropod dinosaurs are an ideal group in which to examine these questions.Theropods were primitively bipedal (Gauthier, 1986; Sereno, 1997) and remainedso throughout their 230-million-year history, thereby freeing the forelimb from asignificant role in terrestrial locomotion. This liberation was accompanied by theevolution of a wide diversity of forelimb morphologies. From a primitive predatorymorphology, at least two lineages evolved highly reduced forelimbs. A third lineagetransformed the forelimb into a feathered wing for generating aerodynamic forcesduring flight (Ostrom, 1976b; Gauthier, 1986; Chiappe, 1995; Chiappe, Norell &Clark, 1996; Padian & Chiappe, 1998). Although over 98% of extant birds use their

  • THEROPOD FORELIMB DISPARITY 151

    Figure 1. Simplified cladogram of Theropoda (after Sereno, 1997). Eoraptor from Sereno et al. (1993);Daspletosaurus from Paul (1988); Deinonychus, Archaeopteryx, and Columba from Chatterjee (1997).

    wings exclusively for aerial flight, several groups also fly underwater, and manyother lineages have become flightless (for a comprehensive review, see Livezey,1995). Herein, we examine forelimb disparity in the morphologically and functionallydiverse clade Theropoda.

    MATERIAL AND METHODS

    Systematics and terminology

    Throughout this paper, we employ the phylogenetic hypotheses of Gauthier(1986), supplemented by the work of Holtz (1994a) and Sereno (1997) for subsequentlydescribed fossil taxa. We follow the cladistic analyses proposed by Chiappe et al.(1996) for basal birds and by Sibley & Ahlquist (1990) for extant birds. All membersof the clade Aves are included in Theropoda. Thus, theropods include the mostrecent common ancestor of Archaeopteryx and all modern birds, as well as all of itsdescendants (Fig. 1). We will use the term theropod to refer to any member of thisclade, both avian and non-avian, unless further restricted. For example, non-aviantheropods will be denoted as such, and bird or avian will be used to refer to membersof Aves (Fig. 1).

    As in our previous study of theropod hind limbs (Gatesy & Middleton, 1997), weagain distinguish taxonomic diversity (number of species) from functional diversity(scope of limb use) and disparity (range of anatomical design or morphologicaldiversity; Gould, 1991: 412; Foote, 1989, 1993, 1997; Wagner, 1995).

  • K. M. MIDDLETON AND S. M. GATESY152

    Data collection

    Lengths of the humerus, radius, and metacarpal II were measured for this study.Although a wealth of non-avian theropods is presently known, the paucity ofspecimens with suYciently complete forelimbs restricted our data set. From theliterature, we collected data for 23 individuals of 20 species (Appendix 1). Thelength of the carpometacarpus was used as the third limb element for birds; lengthsof individual carpal elements were excluded from non-bird measurements. For easeof use, we will refer to the three elements as humerus, radius, and carpometacarpusin both birds and non-avian theropods. Bird forelimbs (Appendix 2) were measuredon specimens housed at the Museum of Comparative Zoology, Cambridge, MA(MCZ) and the Yale Peabody Museum, New Haven, CT (YPM). Wing elementmeasurements were made with either digital calipers or ruler of 543 individualsfrom 324 species of 260 genera in 82 families. Nineteen of the 23 modern avianorders are represented. Additionally, measurements of fossil (32 forelimbs from 28species) and extant birds (78 forelimbs from 46 species) were taken from the literature(Appendix 3). Inclusion of mean lengths allowed the use of additional data frompublished specimens, which often come from fossil deposits in which bones cannotbe associated positively with a single individual.

    Analysis: ternary diagrams

    The lengths of the humerus, radius, and carpometacarpus were added togetherto obtain total forelimb length. Each of the three elements was then divided by limblength to calculate its percentage of the total. Traditionally, bivariate plots havebeen used to study theropod limb morphology and function (Coombs, 1978; Gatesy,1991; Holtz, 1995a). However, interpreting all three variables in such graphs provescumbersome (Gatesy & Middleton, 1997). Ternary diagrams were used to determinethe range of morphological diversity present in theropod forelimb proportions. Suchdiagrams depict the relative contributions of