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Morphological Evolution of the Scapula in Tree Squirrels, Chipmunks, and Ground Squirrels (Sciuridae): an Analysis Using Thin-Plate Splines

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Morphological Evolution of the Scapula in Tree Squirrels, Chipmunks, and Ground Squirrels (Sciuridae): an Analysis Using Thin-Plate Splines EvoIUlion.47(6), 1993, pp. 1854-1873 MORPHOLOGICAL EVOLUTION OF THE SCAPULA IN TREE SQUIRRELS, CHIPMUNKS, AND GROUND SQUIRRELS (SCIURIDAE): AN ANALYSIS USING THIN-PLATE SPLINES DONALD L. SWIDERSKI Museum ofPaleontology, University ofMichigan. Ann Arbor, Michigan 48109 Abstract.-The mammalian scapula, like many bones, is a single structural element that serves as an attachment site for several muscles. The goal ofthis study was to determine whether the scapula evolves as an integrated unit, or as a collection of distinct parts. Shape differences among the scapulae of tree squirrels, chipmunks, and ground squirrels were described using thin-plate spline analysis. This technique produces a geometric description of shape differences that can be decom­ posed into a series of components ranging in scale from features that span the entire form to features that are highly localized. Shape differences among tree squirrel scapulae were found only in large­ scale features, indicating spatially integrated shape change. Chipmunks and ground squirrels differ from tree squirrels in several features, but shared differences reflectingdivergence oftheir common ancestor were found only in the small-scale features. Divergence of ground squirrels from the common ancestor involved some large-scale changes but was dominated by small-scale changes. Divergence of chipmunks was dominated by large-scale changes. Thus, the scapula evolved as an integrated unit during some transitions but as a collection of distinct parts during others. These results suggest that evolutionary patterns of the postcranial skeleton may be as complex as the patterns that have been described for skulls and feeding mechanisms. Key words.-Integration, morphometries, scapula, thin-plate spline. Received April 6, 1992. Accepted March 16, 1993. Ideally, dissection ofanatomy into parts would Thorington 1982, 1984; Hafner 1984; Hight et allow morphologists to predict the units ofevo­ al. 1974; Moore 1959). The closest relatives of lutionary change, the functional elements ex­ the terrestrial lineage appear to be the tree squir­ posed to selection. In reality, this analysis is rels ofthe conservative tribe Sciurini Burmeister, confounded by the complex network of inter­ 1854, which includes Sciurus and Tamiasciurus connections among anatomical parts. The mam­ (Hafner 1984). The relationships of most sub­ malian scapula is a typical example: it is a single genera and many species groups of terrestrial bone, but at least a dozen muscles attach to it. sciurids have also been resolved; figure 1 illus­ Thus, the entire scapula could be expected to trates the relationships ofthe species used in this evolve as a single large unit, or the various mus­ study and represents the combined results ofsev­ cle attachment areas could be expected to evolve eral studies [within tree squirrels (Hight et al. as several smaller units. 1974; Moore 1959), within chipmunks (Leven­ Support for both evolutionary models can be son et al. 1985), and within ground squirrels found in previous studies ofscapular shape dif­ (Gerber and Birney 1968; Nadler 1966)]. ferences. Lehman (1963), Stein (1981), and Tay­ All chipmunks and ground squirrels are less lor (1974) report that localized enlargement of arboreal and more fossorial than tree squirrels specific muscle attachment areas distinguish var­ (Broadbanks 1974; Elliot 1978; Jones et al. 1983; ious specialists from related generalists. Oxnard Lechleitner 1969; Woods 1980). However, many (1968) reports that several orders of mammals of the nesting and foraging traits that comprise exhibit parallel patterns ofshape differences that "arboreality" and "fossoriality" appear to have reflect general factors acting on the whole scap­ undergone multiple independentchanges in both ula. The goal ofmy study is to determine which chipmunks and ground squirrels (Swiderski pattern characterizes the evolution of scapular 1991a). For example, in each genus, the species shape in the Sciuridae. with the largest and most complex burrow sys­ Within the Sciuridae, chipmunks (Tamias) and tems are distantly related (Tamias striatus and ground squirrels (Spermophilus) are members of Ta. minimus;Spermophilus columbianus and Sp. a monophyleticgroup derived from tree squirrels tridecemlineatus). Thus, there are several parallel (Bryant 1945; Ellis and Maxson 1980; Emry and functional transitions in this group. Comparison 1854 © 1993 The Society for the Study of Evolution. All rights reserved. EVOLUTION OF SCAPULAR SHAPE IN SQUIRRELS 1855 oil oil ;, ;, u 0 'c III 0 .! oil oil .. ;, "'0 0 ;, oil 0 > oil - .. oil ;, QI ;, • ·u .;;; oil oil e oil Co ! ;, ;, c: 0 .s ;, oil e .2 oil 0 0 Co 0 ;, "'0 oil oil oil QI QI .. ;, ;, E E .~ III oil e ~ :0 0 QI "'0 •Co 0 oil u u 0 .: QI oil 0 E E oil oil QI .. oil 0 ;, .~ 0 0 QI ;, '0 QI ·c Gi .s 0 III 0 • ..: "'0 ~ :i c E -; -; E .~ 0 'Q. Of ·e 0 U 'c 'e 0 .. .. 'e QI .s- .. u oil 0 ·u 0 Co I- VI vi vi vi I- ~ ~ ~ ~ VI vi vi vi vi vi FIG. I. Phylogenetic relationships ofsciurid species. (See the text for references.) ofthe several transformations ofscapular shape ture the spatial organization Thompson intended should reveal whether there is a general pattern to illustrate. Bookstein (1989, 1991) presents a of integrated change. new technique, the analysis ofthin-plate splines, The currently popular approach to analysis of which produces a rigorous quantitative analysis integration uses multivariate statistics to identify of the spatial organization ofshape change. suites ofcovarying distance measurements (e.g., The analysis of thin-plate splines describes Cheverud 1982; Gould and Garwood 1969; Ris­ shape change by interpolating between the rel­ ka 1986; Zelditch and Carmichael 1989). This ative displacements of discrete points, land­ multivariate statistical approach can be traced marks, presumed to correspond between forms to Olson and Miller (1958), and a bivariate ver­ (Bookstein 1989, 1991). The specific interpola­ sion can be found in Huxley's (1932) analysis of tion function is a mathematical expression for allometry. The conceptual roots lie in D'Arcy the deformation of theoretically idealized thin Thompson's (1917) analysis of shape change, steel plates. This function is not intended to model which sought simple patterns oftransformation biological processes but is chosen because it is affecting entire structures. Thompson's Carte­ smooth and consistent across the entire form. sian grid deformations provided graphic illus­ Consequently, the analysis produces an exact, tration ofglobal components ofshape change but reproducible, and geometric description ofshape were not based on quantitative analyses. How­ differences. In addition, the description can be ever, Bookstein and coworkers (Bookstein et al. decomposed into a series of geometric compo­ 1985; Bookstein 1991; Zelditch et al. 1992) have nents. Each component is a weighted combina­ criticized the traditional statistical analyses of tion oflandmarkdisplacements. The mostglobal distance measurements for their inability to cap- components are combinations that represent 1856 DONALDL. SWIDERSKI 8 patterns of change in the mean shapes of each geometric component. The historical patterns are 7 the basis ofthe subsequent discussion ofthe in­ tegration of scapular shape changes. MATERIALS AND METHODS Shape Coordinates.- Twelve points on each scapula were digitized from video images (fig.2). Most of the points are intersections of ridges or ends ofridges; others are corners. All points were easily identified in all specimens. These consis­ tently recognizable points may be presumed "landmarks," points that correspond across shape changes between taxa (Bookstein et al. 1985; 11 Bookstein 1991). Landmarks are the points at which the biological parts are sampled (Zelditch and Bookstein ms) and the points to which ex­ planations ofshape change are anchored (Book­ stein 1990). Scapulae are not perfectly flat, thus some in­ formation is lost or distorted in the two-dimen­ sional representation ofthese three dimensional objects. In this study, I oriented each scapula with the plane defined by landmarks I, 8, and 9 4 parallel to the plane of focus. The distortion FIG. 2. Scapular morphology and landmarklocations caused by projecting all landmarks onto this plane for the tree squirrel, Sciurus carolinensis: (I) ventral will have greatest effect on the landmarks ofthe end of spine; (2) dorsal end of acromio-c1avicular ar­ acromion and metacromion, which are separated ticulation; (3) ventralend of acromio-c1avicular artic­ laterally from the blade. However, the construc­ ulation; (4) flexure marking the boundary between acromion and metacromion; (5)ventralend of caudal tion of the scapula is fairly simple (two nearly margin of metacromion; (6)dorsalend ofmetacromi­ flat surfaces separated by a strut), and many po­ on-spineboundary; (7)caudalend of vertebralborder, tential effects of changes in lateral position can on teres fossa; (8) intersection of axillary ridge and be easily predicted. Tilting ofthe spine will pro­ vertebral border,between teresfossa and infraspinous fossa; (9) intersection of spine and vertebral border, duce identical antero-posterior displacements of between infraspinous fossa and supraspinous fossa; (10) all landmarks on the acromion and metacromi­ projection ofsubscapular ridge to vertebralborder;(II) on. Tilting of the acromion and metacromion dorsal end of anterior marginal ridge; (12) transition will appear to produce proportionate narrowing between blade and articular process,
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