J・Anthrop・Soc・Nippon人 類 誌、 100(4):391-404(1992) REVIEW ARTICLE Evolution of the Shoulder Girdle with Special Reference to the Problems of the Clavicle Norihisa INUZUKA Department of Anatomy, The University of Tokyo, Faculty of Medicine Abstract Persistent problems involving the clavicle include the reason for its reduction in many mammals, its function in hominids, the last ossification, and so on. In this paper these problems are considered from the point of views of comparative and functional morphology. The clavicle is an element of the dermal shoulder girdle that is in the process of reduction through tetrapod evolution. The reason why the clavicle disappeared or was reduced in cursorial mammals is probably that it disturbed the reciprocal movement of the scapula. The human clavicle works also as a supporter of the forelimb. The characteristic double-curved form of the clavicle may be related to its function. The sternal epiphysis of the clavicle fuses last among the long bones of the human skeleton, in spite of the first ossification of the clavicular body. The delay of determination of the clavicular length should be convenient to slight adjustment for retaining dynamic stability in human bipedal walking. Key Words: Clavicle, Shoulder girdle, Evolution, Comparative osteology, Functional morphology truly homologous to the pubis? Introduction In the present paper I will try to take into There is no bone as peculiar as the clavicle account many factors that may help us to get among the bones that comprise the human answers to the problems about the clavicle. In skeleton. It is the only dermal bone in the order to solve the problems of the clavicle, the postcranial skeleton. Its ossification begins first shoulder girdle must be considered as a whole. and the sternal epiphysis closes last among the The free limbs must be also considered altogether girdle and limb bones. In mammalian forms the to understand the girdles. It is necessary to com- clavicles vary in their presence or absence and pare humans with other primates in order to degree of development. The human clavicle has understand some features of the human shoulder the characteristic S-shaped double curve of girdle. The evolution of mammals, reptiles and primates. Why is the clavicle so peculiar? Some other vertebrates must be followed to know the authors have noted that pectoral and pelvic derivation of their shoulder girdles. Therefore, girdles are serially homologous. Is the clavicle under the title "Evolution of the shoulder girdle" Article No. 9203 Received July 28, 1992 392 N. INUZUKA problems of the clavicle are considered, including the pelvic girdle and free limbs. Dements of the Shoulder Girdle and Their Evolu tionary Trends As the shoulder girdle consists of dermal and endoskeletal elements, each element is separately described following ROMER and PARSONS (1977), KENT (1978), WAKE (1979) and STARCK (1979). The dermal shoulder girdle is derived from the pectoral armor of placoderms. As the cros- Fig. 1. The dermal and endochondral sopterygians took to land, the operculum was shoulder girdle; cl: clavicle, cth: cleithrum, lost; the subsequent loss of the posttemporal, cor: coracoid, gl: glenoid, ic: interclavicle, which was situated most dorsally among the der- pc: procoracoid, pt: posttemporal, sc: scapula, sct: supracleithrum. mal shoulder girdle elements, resulted in the dis- connection of the dermal shoulder girdle from the cranium. The dermal shoulder girdle includes have a tendency to become reduced. It is con- the posttemporal, supracleithrum, postcleithrum, cluded that the dermal elements as a whole have cleithrum, clavicle and interclavicle (Fig. 1). a tendency to become reduced or disappear. Among these elements, all except the interclavicle The endoskeletal shoulder girdle lies within were originally present and only the interclavicle and behind the dermal girdle and bears the appeared after the transition to land (ROMER glenoid fossa (ROMER and PARSONS, 1977). The and PARSONS, 1977). The dorsal elements (post- endoskeletal girdle includes the scapula, pro- temporal, supracleithrum, and postcleithrum) are coracoid and coracoid (Fig. 1). The scapula is well developed in aquatic forms but tend to be present above the glenoid fossa, and the others reduced in terrestrial forms. Table 1 shows the are below it. The procoracoid is also called the presence or absence of the ventral elements epocoracoid and the coracoid is also called the (cleithrum, clavicle and interclavicle). According metacoracoid. Table 2 shows the presence or to the table, even the ventral dermal elements absence of the endoskeletal shoulder girdle. Table 1. Distribution of features of ventral elements of the dermal shoulder girdle; 0: presence, x : absence Evolution of the Shoulder Girdle 393 Table 2. Distribution of features of the endochondral shoulder girdle; 0: presence,* : fuse, x : absence According to the table, the scapula never dis- Finally, no matter what the actual ossification appears, but instead develops. To the contrary, pattern is, the clavicle of eutherians, including the ventral elements of the endoskeletal girdle humans, is truly homologous to the original have a tendency to become reduced. The dermal dermal shoulder girdle. The reason why only the girdle is more developed than the endoskeletal clavicle among the postcranial skeleton derives girdle in aquatic fishes and is less developed in from dermal bone is that only one bone survived terrestrial tetrapods. The reason why such a among the many original dermal elements, and condition occurred is that the caudal margin of that the clavicle was originally a part of the the gill opening must be hardened in fishes and dermal cranium in spite of being a part of the that tetrapods need many more girdle muscles "shoulder girdle" in human anatomy . As MIKI because of the transformation of the main (1981) expressed it, "the dermal shoulder girdle locomotory organ from the trunk to the limbs. was a remnant of the posterior margin of the There have been many opinions about whether helmet in armored fishes." the ossification pattern of the human clavicle is really dermal or endochondral. According to The Evolution of the Shoulder Girdle in a LESSERTISSEURand SABAN (1967), HUXLEY, Functional View SABATIER, BROOM, FAWCETT (1913), 1. Early tetrapod stage: lateral type limb ANTHONY, WATSON, HANSON and ROMER The early tetrapods and amniotes have preferred a dermal origin, while GEGENBAUR, laterally oriented limbs. REWCASTLE(1981) calls GOETHE, HOFFMAN, TODD and d'ERRICO it "sprawling limb posture" . The "lateral" type (1928), and KOCH (1960) preferred an endo- limb is also called the "horizontal" or "trans- chondral one. In a third view the clavicle is con- verse" type. LESSERTISSEURand SABAN (1967) sidered a combination of both, but the relation separate the advanced "type horizontal" from between dermal and endochondral bones is the more primitive "type transversal" , but I unite variously understood. For example, according to them as the lateral type; they are common in LESSERTISSEUR and SABAN (1967), FITz- having the stylopodium protruding horizontally WILLIAMS referred to the clavicular body as from the trunk. Bodies with the lateral type limb dermal bone and only to the sternal end as endo- develop adductor muscles which run from the chondral. APOSTOLAKIS(1934) referred to the ventral part of the joint of girdles to the humerus body as dermal bone and to both ends as endo- and femur in order to bear the trunk off the chondral. GARDNER (1968) said that the clavicle ground. The amphibians and early reptiles walk ossified without a cartilaginous stage, but that by moving both stylopodia fore-and-aft in a cartilage occurred late on both ends. horizontal plane for their lateral type limbs . This 394 N. INUZUKA movement enlarges the area of muscles in the type. Actually the transformation was established pelvic girdle which protract and retract the limbs. by rotation of the elbow backward and of the Thus, in both girdles the area ventral to the knee forward. joint with the stylopodia becomes broader than There have been some theories about the the dorsal area, and the area anterior to the joint reason why the stylopodia in fore- and hindlimbs extends forward and the posterior area backward. rotated in opposite directions: for example, in an "Both pectoral and pelvic girdles can be reduced animal that extends its limbs outward from the to a common pattern, of one dorsal and two trunk, it is dangerous when a predator attacks, ventral elements" (YAPP, 1965). Therefore, the or it conserves body heat to hold the limbs under clavicle is not homologous to the pubis but the trunk, or it is better for walking on narrow analogous to it. branches (MATTHEW, 1904; GREGORY, 1910; While the shoulder and the pelvic girdles BOKER, 1935). But amphibians and reptiles converged on a common pattern, they were to retain the lateral type limbs even now, notwith- take a contrasting shape in their connection with standing the presence of many predators. It does the axial skeleton because of the presence of the not seem to have been so cold as to require the thorax. That is, the shoulder girdle unites with animals to conserve body heat, when and where the thorax via the clavicle or the interclavicle (lost the "mammal-like reptiles" evolved the inferior later and changed to the sternoclavicular joint), type limbs. And there is no evidence that they and the pelvic girdle unites with the sacrum via were arboreal animals. the ilium by a bony connection. The shoulder The most important reason for the trans- girdle forms a striking contrast to the pelvic girdle formation from the lateral to the inferior type in the relative position of its bony connection between the axial skeleton and the articulation with the limbs: it is more ventral in the shoulder girdle and more dorsal in the pelvic. In other words, the body weight hangs from the shoulder girdle in the anterior half of the body and rides on the pelvic girdle in the posterior half.