Vertebral pathology in the Afar australopithecines

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 6083-101 (1983)

Vertebral Pathology in the Afar Australopithecines DELLA COLLINS COOK, JANE E. BUIKSTRA, C. m A N DEROUSSEAU, AND D. CARL JOHANSON Departmmt of Anthropology, Indiana University, Bloomington, Indiana 47405 (D. C.C.), Department of Anthropology, Northwestern University, Emnstim, Illinois 60ZOl (J.E.B.), Lkpar&tment of Anthmpology, New York University New Ywk, New York loo03 (C.J.DeR.), Cleveland Museum of Natural History, Cleveland, Ohio U106 D.C.J.), and Institute of Human Origins, Bwkeley, Cal@rnia, 947’04

Early hominids, Scheuermann disease, Spine, KEY WORDS Australopithecine

ABSTRACT Ten vertebral elements from the AL-288 partial hominid skeleton and 11 elements from the AL-333 collection are described. The AL-288 column presents a marked kyphosis at the level of thoracic vertebrae 6 through 10, with pronounced new bone formation on the ventral surfaces of these vertebrae. These features, associated with narrowed disc space and minor osteophytosis, resemble Scheuermann disease in the human. Even though this diagnosis is consistent with a basically human, bipedal locomotor repertoire, the presence of Scheuermann disease suggests that lifting, climbing, or acrobatic activities may have been important in early hominids.

The vertebral column of Plio-Pleistocene hominids is becoming well represented in fossil collections. Sterkfontein has yielded two isolated vertebrae, as well as the Sts-14 partial column (Robinson, 1972). There are three specimens from Swartkrans (Robinson, 1970, 1972) and three as yet undescribed vertebrae from East Turkana (Walker and Leakey, 1978).

The new finds from the Pliocene Hadar formation in Ethiopia nearly double the number of early hominid vertebrae available for study. The AL-333 locality has produced nine isolated vertebrae, and the AL-288 “Lucy” partial skeleton includes 15 vertebral elements (Johanson, White, and Coppens, 1978; Johan- son et al., 1982; Lovejoy, Johanson, and Cop- pens, 1982). The AL-288 vertebrae show several unusual pathological features. This paper describes these features and explores their implications for locomotor and other functions of the spine in the australopithecines.

First, we describe the 24 vertebrae, placing emphasis on features related to interpretation of pathological changes. We then isolate two syndromes-one an anterior expansion of the vertebral body that may be a normal phenomenon in australopithecines, the other a more pronounced expansion related to degeneration of the intervertebral discs in AL-288. Al-

though the first is probably developmental, the other is clearly pathological. Behavioral implications of theses two syndromes are then explored.

MATERIALS AND METHODS

Age, sex, and identi;ficaticm of elements AL-288: Age, sex, and region of involvement

are important in differentiating pathological conditions affecting the spine in modern humans. Although inferences about the age of fossil hominids must be tempered by a recog- nition that the rate of age change is unlikely to have been the same as in Homo sapiens, skeletal age indicators in AL-288 are consistent with a developmental stage comparable to the close of the third decade of life or the beginning of the fourth in modern humans. It appears that Lucy was approaching middle age. We base this opinion on the following features of the AL-288 specimen:

1. The third mandibular molars are erupted. While occlusal attrition on these teeth is slight,

Received February 9,1982; accepted July 16,1982.

‘Howell no longer considers the Omo lumbar vertebra L 106-7 (Howell and Coppens, 1974 12) to be a hominid (Howell, personal communication), and we concur in this opinion.

oooZ-9483/83/60010083$05.50 0 1983 ALAN R. LISS, INC.

84 D.C. COOK, J.E. BUIKSTRA, C.J. DEROUSSEAU, AND D.C. JOHANSON

the wear gradient across the molars is high, and interproximal wear on the third molars is pronounced. This pattern suggests that the maxillary opponents of the third molars were not in full functional occlusion.

2. Ring epiphyses of all vertebrae are united, but their margins are still distinct. Epiphyseal lines in the longbones are faint or absent. These features are consistent with an age in the 20s or 30s.

3. The centra of the first and second sacral vertebrae are incompletely united, a condition seldom seen after age 30 in modern humans.

4. The pubic symphysis shows prominent ventral lipping, some breakdown, and some rim fomation, as well as retention of Faint ridges and furrows, suggesting an age of 30 or above in modern humans. This mixture of features is consistent with the advanced and irregular pattern of age change often encountered in parous human females.

AL-288 is quite small. Afar hominids are di- morphic, in both dental and postcranial features, as Johanson and White have pointed out. For these reasons, AL-288 is most probably female (Johanson and White, 1979).

The AL-288 vertebrae correspond to those of modern humans in remarkable detail. If they are identified according to the same diagnostic morphological features as in modern humans, the elements listed in Table 1 are present. The vertebrae do not correspond in morphological detail to chimpanzee or other nonhuman primate vertebrae; hence our use of analogy to modern humans in identifying these elements is the only appropriate one. However, reser- vations like those Robinson (1972) has ex- pressed concerning Sts-14 are appropriate here. Because there are missing elements, we cannot be sure that segmentation of the column was the same as in modern humans, and the element we identify as TV-12 here might be better considered the ultimate element in a thoracic spine of indeterminate length. We have checked the identification by metric ap- proximation of the missing lumbar elements (Fig. 1). Dimensions for the AL-288 vertebrae are plotted according to the element identifications presented in Table 1. If there were six lumbar elements in AL-288, as there are in Sts-14, plotted values for T11 through T6 should be shifted to the right. If there were four lumbar elements, as is usual in pongids, these values should be shifted to the left. How-

'The cornrnun pattern of vertehral segmentation ih pongiilh in 13 lhwacicr iuid tiiur lunibws. whereas humans commonlv have 12

ever, the correspondence of the AL-288 data and the shaded range of values observed in modern humans is best if five lumbar vertebrae are assumed and if AL-288-1AK is identified as a second lumbar. A similar analysis of small samples of pongids indicates that the lumbar and lower thoracic vertebrae are more homomorphic in the three dimensions considered here than is the case in AL-288 or Homo snpiens. Note, however, that AL-288 is relatively homomorphic in the anterior-posterior diameter of the superior ring epiphysis when compared with modern humans. We have elected to assume that there were 12 thoracic elements because the alternatives to this no- tation are exceedingly cumbersome.

Fig. I. Serial changes in vertebral dimensions in A L 288 (circles) and in seven modern human spines selected to include individuals of small body size. Transverse breadth on the superior ring epiphysis (SST), anterior-posterior breadth on the superior ring epiphysis (SSAP), and anterior body height (ABH) are shown. All scales are gradu-

thoraeics and five lumbars. ated in centimeters.

AUSTRALOPITHECINE VERTEBRAL PATHOLOGY 85

TABLE 1. Identification of vertebral elements in AG288 and AL333 collections

1 AH 1 AF 1 AG

Thoracic vertebra 6 Thoracic vertebra 7 Thoracic vertebra 8

1 AD 1 AC 1 A1

Thoracic vertebra 10 Thoracic vertebra 11 Thoracic vertebra 12

AL-288 1 AM Thoracic vertebra 3 or 4 Partial neural arch. Superior and inferior facets are greater

in transverse than in craniocaudal diameter. They are small with respect to the zygapophyses. There is a depression caudal to the superior facets not found on lower cervical vertebrae in H. sapiens. Spinous process is angled about 489Nith respect to the neural canal

Complete except for spinous process. Vertebral body. Complete except for anterior and half of superior surface of

body, spinous process, left pedicle, and transverse process. Vertebrae 1 AH, 1 AF, and 1 AG articulate with one another, but do not articulate with 1 AD; 1 AG and 1 AD are similar in size and shape, suggesting that only one element, TV 9, is missing.

Essentially complete. Inferior costal demifacet is absent. Essentially complete. Right pedicle, costal facet, zygapophyses, transverse process,

and lateral portion of lamina. Vertebrae 1 AD, 1 AC, and 1 A1 can be articulated with one another, and 1 A1 is the transitional vertebra, having a superior facet that is thoracic in morphology and a lumbarlike inferior facet. The anticlinal vertebra is usually TV 12 in humans and is thoracic in primates in general (Ankel, 1972: 239). If segment 1 A H through 1 A1 is moved upward by assuming that 1 A1 is TV 10 or 11, 1 AH is moved to a point in the column where it fails to correspond to body and neural arch proportions usual in H. sapiens (See Fig. 1).

appropriate to LV 2, relative to body size. Anterior body height is only slightly greater than posterior body height (see Fig. 1).

suggests that it is distal to 1 AK but too large to correspond to the usual form of LV 5 .

1 AK Lumbar vertebra 2 Essentially complete. Interzygapophysis diameters are

1 AB Lumbar vertebra 3 or 4 Spinous process and medial portions of laminae. Shape

1 AN Sacral vertebrae 1-5 Essentially complete sacrum, showing substantial distortion.

AL-333 x-12 Thoracic vertebra 10 Essentially complete; ring epiphyses not fused at time of

death. Inferior demifacet for head of rib is present but articular facet for tubercle of rib is absent, as in 1 AD and most human TV 10.

W - 8 Sacral vertebra 1 or I,V 5 Anterior surface of vertebral body. Body is broad and posteriorly wedged.

51 Thoracic vertebra 7. 8. or Body. Proportions of body and profiles and comparable to TV 9 7 to 9 in-H. sapiens and AL-288.

73 Lumbar vertebra 3 Body. Same. 81 Thoracic vertebra 2 Body, right and left pedicle, and left prezygapophysis. Body

is wide and low, and superior surface is deeply indented, as in H. sapiens. Ring epiphyses are not united.

83 Cervical vertebra 1 101 Cervical vertebra 2 Fragmentary. 106

Left lateral mass and lateral half of posterior arch.

Essentially complete. Transverse process guttered and Cervical vertebra 5 or 6 foramen small.

w- 14 CV5, 6,7, TV 1 or 2 Spinous process.

AL-333: The nine isolated vertebrae from AL-333 include both large and small elements so distinct in size as to suggest the same marked dimorphism noted by Johanson and White in other parts of the skeleton (1979). Some specimens are subadult as indicated by incomplete fusion or absence of the ring epiphyses. Identifications of the AL-333 elements

based on reference to the AL-288 specimen and to modern human samples appear in Table

1lESCRIPTION 1.

We approach these materials using two methods: first, detailed description of pathological alterations visible on the specimens, and second, differential diagnosis.

86 D.C. COOK, J.E. BUIKSTRA,C.J. D IEROUSSEAU. AND D.C. JOHANSON

General morphology

Although a general description of the Hadar vertebrae is outside the scope of our project, we will point out features of the general morphology of these specimens that are important in our biobehavioral interpretation of the pathological changes. The Hadar vertebrae depart from the morphological pattern found in modern humans in a few details that may

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have functional significance. Cervical spinous processes in the AL333 specimens are quite long, and the base of the spinous process on AL-288-1AM upper thoracic vertebra is well developed, suggesting that the spinous processes may have been massive at this level as well. The length and rugosity of the spinous processes indicate that the erector spinae complex, rhomboids, and trapezius were massive relative to their size in modern humans.


As Robinson (1972) has pointed out in Sts- 14, the vertebral bodies in the thoracic and lumbar spine are quite small with respect to the size of the neural arch. This is true in all

Hadar specimens for which both parts of a given element are present (Fig. 2). The relationship is in part a matter of allometry, because the neural canal is relatively large in

n

Fig. 2. Thoracic and lumbar vertebrae of AL-288. In the accompanying schematic drawings, new bone formation related to the area of attachment of t h p anterior longitudinal ligament is indicated with diagonal lines, new bone formation on the intervertebral facets with horizontal

lines, and missing portions of the vertebrae with dashed lines. Missing portions are reconstructed as an aid in read- ing the photos and may not fully represent the origiiial form. Letter8 on the ring epiphyset; coryesgond to the last digit of the specimen in Table 1.


small individuals, and AL-2% and Sts-14 are small indeed. However, the much larger AL- 333x-12 thoracic vertebra 10 from Hadar shows the same proportionately long transverse processes and robust neural arch despite the relatively small neural canal, suggesting that allometry alone is not an ade- quate explanation for the small vertebral bodies present in the available australopithecines. I t seems more plausible that the robust neural arch also reflects a well-developed dorsal musculature.

The ring epiphyses of AL-288 are more extensive than is usual in modern humans. Sev- eral vertebrae show a thin, incomplete layer of bone extending across the intervertebral surfaces of the centrum, separated from the underlying cancellous bone by an interval of somewhat less than a millimeter. Such paper- thin extensions of the ring epiphysis are com. mon in pongids, and represent a condition in. termediate between the ring epiphysis of humans and the continuous epiphyseal plate found in quadrupedal mammals. In humans the intervertebral endplates are largely com- posed of hyaline cartilage. The portions of this cartilage layer adjacent to the body are calci- fied, forming an extremely thin, discontinuous cortex that is not separated from the body by uncalcified cartilage (Bradford and Spurling, 1945; Donohue, 1939).

Descri;otion of pathological changes AL-288: The sacrum, sacroiliac joints, and

peripheral joints of AL-288 show no significant pathological changes. The absence of marginal ossifications of the joint capsules in the appen- dicular skeleton is striking in view of the frequency with which such minor lesions are seen in relatively young adult humans. Lovejoy (personal communication) has pointed out that AL-288 has small medial-superior osteophytes into the muscle attachments on the greater trochanters of femur. These features show no abnormalities of surface texture, and we re- gard them as within the normal range of vari- ation encountered in Homo sapiens.

On the second lumbar vertebra AL-288-1AK, there is limited new bone formation on the ventral surface of the body corresponding in location to the anterior longitudinal ligament (Fig. 3). This tissue consists of highly vascular woven bone, and is less compact than other areas of the cortex. I t has well-defined margins. While the new bone formation is not sufficient to alter the superior profile of the vertebral body (Fig. 21, there is a somewhat thickened nodular elevation in the new tissue which is confluent with the inferior ring epiphysis and contributes to the smooth marginal osteophyte. This thickened area of new bone formation contributes to a slight keeling of the vertebral body. Fine, dense, smooth marginal osteophytes arise from the ventral aspects of both ring epiphyses (arrows in Fig. 2), reach- ing a thickness of about 4 mm in the midline.

The intervertebral facets of the second lumbar vertebra are lipped to a very slight degree.

A n

Fig. 3. Ventral view of AL-288-1 AK. There is woven bone (diagonal shading in schematic) corresponding in location to the anterior longitudinal ligxment, as well as lipping of the inferior intervertebid facets. Superior facets also show some lipping (Fig. 2).


Superior facets expand beyond their normal articular surface about 2 mm on the left and 3 mm on the right. Inferior facets extend cau- dally about 0.5 to 1.0 mm beyond their original margins. This lipping is oriented in a craniocaudal direction, suggesting the ventral flexion of the spine was a contributing activity. Supe- rior sacral facets are also lipped, the osteophytes extending about 1 mm from the original cranial borders of the facets.

These very minor pathological changes are present to a much greater degree in the lower thoracic vertebrae of AL-288. There is pronounced new bone formation on the ventral surface of all the preserved thoracic vertebral bodies, beginning at the level of the cranial half of the tenth thoracic vertebra and extending through the sixth, where the contiguous series of preserved elements ends. These lesions correspond in location to the anterior longitudinal ligament. New bone formation is greatest at the level of the eighth thoracic vertebra as judged from the contours of the adjacent elements (Fig. 2). In contrast, the zygapophyses show only minor pathological changes.

New bone formation on the ventral surface of the body of the 11th thoracic vertebra has much the same character as that on the second lumbar, except that the tissue in the former expands the dorsoventral diameter of the body perceptibly (Table 2). The superior marginal osteophyte is less regular and smooth than that of the second lumbar vertebra. There are elevations at the lateral inflection points of the superior margin of the body corresponding to

the margins of the anterior longitudinal ligament. Fine radially arranged grooves produce an undulating surface on the cranial aspect of the osteophytic new bone. The superior marginal osteophyte is directed anteriorly or ventrally rather than across the intervertebral disc. Whereas the ventral margin of the osteophyte consists of condensed, smooth bone, the tissue comprising the portion of the superior surface of the body that projects beyond the ring epiphysis consists of very fine, uniform trabecular bone deposited in concentric striae. There is pronounced wedging of the body, both at the level of the ventral limit of the ring epiphysis and at the ventral border of the osteophyte (Table 2). Intervertebral facets show no lesions.

At the level of the tenth thoracic, AL-288- lAD, new bone formation under the anterior longitudinal ligament becomes pronounced, forming a projecting, irregular osteophyte at the superior margin. New bone formation is thickest on the ventral surface; however, the most distinct, projecting osteophytes are anterolateral in orientation. Extension across the disc space in the annulus fibrosus is more pronounced at the superior margin of the tenth thoracic than at any other location in the preserved portions of the AL-288 spine. The body is wedged (Table 2), and there is a slight asym- metry in the new tissue such that the osteophytes are larger on the right than the left. This probably reflects aortic deviation. There are depressed, irregular radial grooves on the superior surface of the new bone. There is little significant change in the intervertebral

TABLE 2. Vertebral body dimensions in AL288 and A M 3 3 specimens

Superior ring epiphysis breadths Anterior/ Body heights on ring epiphysis Mitlbodv posterior

Specimen Element Transverse Anterior/posterior diameter %increase' Anterior Posterior

AI,-2881AH AL-288-1AF AL-288-1AG AIrZIBl-AD AIr2881AC AL2881AK AIA88-1AN AIS333~-12 A L - 3 3 3 ~ 4 AL-333-51 AL-333-73 AL-333-81

TV6 m7 W 8 m 10 m 1 1 LV2 SV1-5 TVlO SV1 or LV5 TV7, 8, or 9 LV3 TV2

16.6 16.5 - 19.2 22.5 29.7est 34.3est 26.0

24.9 34.5e~t 13.3

-

13.8 13.8 15.5 14.9 17.6 17.lest 17.9 19.7 - 17.0 22.5est 14.2

21.7 22.2 -

20.4 1'3.0 15.8

19.0

20.1 20.5 14.1

-

-

57 61

40 8 0

0

18 0 0

-

- -

12.1 11.9 13.3 13.1 13.8 19.3 21.5est 12.6

17.1 24.9 11.4

-

13.3 13.6 13.6 14.5 i6.5 21.6

14.8

18.5 24.4 12.2

- -

'A rough estimate of the increase in anteriorlposterior vertebral diameter is calculated by suhtraeting the AIP diameter on the superior ring epiphysis from the midbody AIP diameter and expressing the difference as a percentage of the AIP diameter of the superior ring epjphysis. This increase is largely attributable to proliferation under the anterior vertebral ligament. An attempt at estimating the thickness of this tissue rddiographicalIy failed because the bone and matrix are equally drnxe and opaque.


facets; however, the inferior margins of the inferior facets are well defined and may reflect some expansion (Fig. 4).

Proliferation under the anterior longitudinal ligament can be followed on the eighth, seventh, and sixth thoracic vertebrae. Lesions on these vertebrae are relatively similar and can therefore be described together. Proliferative

new bone in AL-WlAH, lAF, and 1AG is coarse, highly vascular, and irregular in texture. It is most extensive in the midline, forming a distinctive keel (Fig. 2). The osteophytic new bone shows some aortic deflection. On the sixth thoracic vertebra, the caudal surface is damaged, exposing the trdbeculae immedi- ately beneath the compactum. The new bone

Fig.. 4. Oblique views of the inferior surfaces of the tenth (1 AD) and eleventh (1 AC) thoracic rlcments in AI,-288, showing lipping of the intervertehral facets. Area intlicatc~l in black on AL-288-1 AC is hrokrn auay, hut the base of the facet remains. Inferior miirgiii of the left faccxt \ c i s much larpcv and moi.c projecting. than on the right.


is organized in concentric layers, presumably reflecting gradual, episodic formation. The coarse, irregular trabeculation characteristic of osteophytosis in modern humans is not seen (Fig. 2). In all three vertebrae, preserved anterior portions of the proliferative tissue are rough and have a woven appearance. On the lateral aspects of the vertebral bodies, the cortex becomes less striate and irregular in a graduaI manner, and is smooth near the costal facets.

There is clear evidence for a pronounced k y phosis at the level of thoracic vertebrae 6 through 8. There is some wedging of the vertebral bodies, anterior heights on the ring epiphysis being substantially lower than posterior heights taken in the midline, and heights at the ventral border of the body being proportionately reduced as well (Table 2). Corre- sponding osteophytes on the sixth and seventh elements are fully congruent (Fig. 51, indicating that the intervertebral disc had collapsed at this level. When the corresponding surfaces are approximated, the height of the disc at the level of the ventral margin of the ring epiphysis can have been no more than 2 mm. The irregular surfaces of the adjacent osteophytes on the sixth, seventh, and eighth elements are congruent across the disc space, indicating that this space was much reduced at the level of both these interspaces. A similar irregular rip- pling appearance of the proliferative tissue on the superior surfaces of the tenth and sixth elements and on the inferior surface of the eighth element suggests that the discs had herniated forward from the level of interspace

5-6 through interspace 9-10 at minimum. This extensive disc disease must have resulted in a marked kyphosis.

Osteoarthritic changes in the intervertebral facets are limited to extremely minor lipping or rounding of the margins of the articular surfaces. There is no fusion of adjacent osteophytes or zygapophyses, and the predominant direction of new bone formation is anterior rather than craniocaudal. There is no effusive ossification of the annulus fibrosus. No Schmorl nodes-herniations of the nucleus pulposus into the vertebral body-are present at any of the levels where such lesions could be observed.

AL-333: The AL-333 vertebrae represent several individuals differing in both size and age a t death. We will limit the description of lesions in these materials to observations that we feel shed some light on the lesions seen in the AL-288 specimen.

The juvenile tenth thoracic element AL- 333w-12 shows no lesions apart from osteoarthritic lipping of the right costal facet. This specimen corresponds in developmental age to early adolescence in modern humans. The ring epiphyses are unfused, as is the epiphysis of the spinous process. The epi hyses of the

surfaces of the bodies are billowed as is usually seen in modern humans at this age. The outline of the body corresponds to that of the ring epiphysis of AL-288-1AD in shape rather than to the shape produced by the tissue we

transverse processes are fused: Y Craniocaudal

Fig. 5. Lateral and ventral views of AIA88.1 AH and 1 AF tihowiiig congruent oht rophyt~~.s .


have identified as proliferation under the anterior longitudinal ligament.

The adult midthoracic vertebra AL-333-51 consists of a vertebral body including the costal facets. w e saw only a plastic cast of this specimen, and our observations are necessar- ily limited, despite the excellent quality of the cast. There is a narrow band of new bone formation in the midline on the ventral surface of this vertebra. It is highly vascular and somewhat irregular in surface. Borders are indistinct, the lesion tissue merging gradually into the normal cortex at the area of greatest flexure between the ventral and lateral surfaces. The superior margin shows osteophytic lipping in a ventral and caudal direction (Fig. 6). Lipping is limited to the anterior two thirds of the ring, and is most pronounced at the anterior limit. The inferior margin shows ven-

.'I-\

tral and lateral lipping that is most pronounced at the costal facets. The ring epiphyses are consolidated to approximately the same extent as in the AL-288 specimen. Ring bone is still distinct, and has a circumfer- ential fiber orientation. Trabeculation in the proliferative tissue is ventrally or radially directed. There is no extension of osteophytes across the annulus fibrosus.

The adult lumbar vertebra AL-333-73 and the adolescent thoracic vertebra AL-288-81 show no lesions of any consequence.

DISCUSSION Patterns in th.e Hadar vertebral lesions

We distinguish two patterns in the lesions we have described. The first of these is the very modest expansion seen under the anterior vertebral ligament in AL-333-51, and per-

Fig. 6. Cranial and lateral views of AI,-&B51 (cast). See key to schematic drawings in Figure 2


haps some portion of the extreme expansion seen at this location in AL-288. This minor expansion may be a normal developmental phenomenon. Both the published photographs (Robinson, 1972) and the Wenner-Gren casts of elements from Sts-14 show similar ventral expansion of the lower thoracic vertebral bodies beyond the ring epiphysis. Since all three available midthoracic vertebral columns of adult australopithecines show some expansion of this kind, we argue that this was a normal feature in these early hominids. We have seen similar ventral expansion of the vertebral bodies beyond the limits of the ring epiphysis in adult chimpanzees, orangs, and macaques. Comparison of adults of these species with juveniles, and of AL-288 and AL-333-51 with the juvenile AL-333w-12, suggests that fusion of the ring epiphysis occurs well before the completion of ventral growth of the vertebral body. The Hadar specimens are similar to pon- gid vertebrae in very few features; however, the extent and thickness of the ring epiphyses are more like the usual condition in pongids (Fig. 2) than that seen in modern humans. Ventral growth beyond the margins of the ring epiphyses is rare in modern humans, and we have seen examples only in the lumbar spine. Ericksen views increase in both transverse and anteroposterior body breadths as a constant feature of aging in modern humans, and her work documents continued growth in these dimensions in the lumbar vertebrae (1976, 1978a). If similar change occurs in the lower thoracic spine in modern humans, it is much more subtle, and seldom produces the appearance seen in pongids or the australopithecines. However, when rapid growth in the vertebral bodies does continue after the fusion of the ring epiphyses in humans, as for example in acromegaly, expansion as pronounced as that seen in AL-288 can result (Epstein, 1955: 168-170; Jaffe, 1972: 335).

The second pattern we can distinguish in the Hadar material is the group of very marked alterations in vertebral morphology that we have described in AL-288. These changes include loss of disc space in the lower thoracic spine, wedging of the vertebral bodies in this region, kyphosis, and ventral expansion of the bodies of the affected vertebrae. Synovial joint involvement and ossification of the annulus fibrosus are very minor. These are clearly pathological changes, and the most useful way to explore them further is to attempt a diagnosis.

There are many difficulties in applying modern diagnostic labels to these lesions. The aus-

tralopithecines are removed from modern humans in both phylogenetic distance and in time. Diseases present today may not have existed more than 3 million years ago, and diseases present then may have disappeared. However, with these limitations in mind, applying a differential diagnosis can help us un- derstand the factors that may have contributed to the lesions in the AL-288 spine.

Diflerential diagnosis The list of conditions that appears in Table

3 is the result of a survey of the relevant medical literature for all conditions producing lesions in any way similar to those in AL-288. Features of AL-288 appear at the left of the table.

In the septic arthritis syndromes-including tuberculosis, pyogenic osteomyelitis, osteitis of the spine, and the bone mycoses-focal destructive lesions are prominent, and there is generally evidence of periosteal repair. Re- gional or general osteoporosis is also common. In early lesions resulting from both pyogenic and nonpyogenic infections of the spine, erosion of the craniocaudal surfaces of the vertebral bodies may be present in the absence of the more pronounced changes just discussed (Genant, 1979: 123-124). The AL-288 lesions do not fit this pattern.

The inflammatory arthritis syndromes include ankylosing spondylosis, psoriatic spondylosis, Reiter syndrome, enteropathic arthritis, ankylosing hyperostosis, and rheumatoid arthritis. All are characterized by profuse calcification and ankylosis of the annulus fibrosus, as well as by calcification of ligamen- tous attachments. The intervertebral disc space is usually preserved (Jaffe, 1972: 779- 840; Epstein, 1955: 190-191; Genant, 1979). Genant groups the first five of these together because they are associated with the HLA- B27 antigen, and because they share several jointly pathognomic features. In all five, ossifications into the annulus fibrosus are craniocaudal in orientation (syndesmophytes) rather than dorsoventral in orientation (osteophytes). All five are characterized by profuse ossifca- tion of the peripheral ligaments and muscle attachments-in Genant’s terminology, entheseopathy.

The HLA-B27 linked syndromes are partic- ularly distinctive when compared with the degenerative disc disease usually seen in senile or use-related o~teoarthrit is .~ Moskowitz “WQ use the term osteoarthritis in the unitary sense, embracing

senile or use-related degenerative disc disease and degenerative joint disease.

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Scheuermann disease

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Neuropathic joint disease

Spondyloepiphyseal dysplasia

Ankylosing arthropathy of vitamin-D-resistant rickets

Ochronosis

Mucopolysaccharidoses

Acromegaly

Rheumatoid arthritis

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Reiter syndrome

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(1979: 1174) says of ankylosing hyperostosis that

Specific criteria for vertebral involvement, which allow differentiation of this disease from degenerative disc disease and ankylosing spondylitis . . . included “flowing” ossification along the anterolateral aspect of at least four contiguous vertebral bodies, pres- ervation of disc height, absence of vacuum phenomena or vertebral body sclerosis, and absence of apophyseal joint ankylosis or sacroiliac joint erosion, sclerosis, or fusion.

Similarly, sacroiliitis and syndesmophytosis are sufficient diagnostic criteria for ankylosing spondylitis (Bluestone, 1979: 621), Reiter syndrome and psoriatic and enteropathic arthritis. The latter conditions are differentiated from ankylosing spondylitis on the basis of the lesion associations that give them their names and on the degree and character of the syndesmophytes (Genant, 1979: 98-107).

Rheumatoid arthritis is unlike the other inflammatory arthritis syndromes in being primarily a disease of synovial membrane that results in largely destructive changes in bone. Preceding the destructive or erosive lesions, there is often profound loss of bone density in the affected joints. Destructive lesions result in subluxation and loss of normal joint archi- tecture. This joint disruption ends in fusion in only a minority of cases, and fusion of elements in the spine is uncommon. Destruction of the vertebral bodies and erosion of the vertebral endplates precedes loss of disc height (Genant, 1979: 79-91). None of these inflammatory arthritis syndromes resemble the AL- 288 lesions in more than a fe-7 isolated features.

Acromegaly, the mucopolysaccharidoses, ochronosis, vitamin-D-resistant rickets, and spondyloepiphyseal dysplasia are a very diverse group of congenital or acquired conditions that share at least some features with the AL-288 lesions. However, it is clear, as shown in Table 3, that none of these relatively uncommon conditions is similar to the AL-288 lesions in overall appearance.

The remaining common causes of lesions of the spine listed in Table 3 are in a more or less direct sense traumatic in nature. The neuro- trophic joint diseases are characterized by massive mechanical disruption of joints and by patterning related to sensory supply. The AL-288 spine presents no evidence for these conditions. There is no fragmentation of the vertebrae in the AL-2% specimen, and marginal osteophytosis is limited. Subluxation is also absent.

A second condition with traumatic associations is degenerative joint disease, the most common of the arthritis syndromes. While there is controversy in the medical literature concerning the relationship of given activities to the development of degenerative joint disease, most authorities agree that low level traumata contribute to its etiology (Moskow- itz, 1979; Jaffe, 1972; Sokoloff, 1969; Epstein, 1955). We follow Jaffe (1972: 762) in consider- ing degenerative disc disease, spondylosis deformans, or spinal osteophytosis as an aspect of degenerative joint disease. In modern humans, degenerative joint disease is seldom prominent before the age of 40, and in the spine it generally is most pronounced in the lower portions of each spinal region, especially in the penultimate vertebrae (Stewart, 1947; Abrams, 1960: 825). Genant (1979: 112) stresses the frequency with which lesions are found in all regions of the spine and the diagnostic value of the association of loss of disc space, osteophytosis, and lesions of the zygapophyseal joints.

Anthropologists have devoted more atten- tion to the relationship between habitual activity and degenerative joint disease than have medical researchers (Angel, 1966; Ortner, 1968; Straus and Cave, 1957; Stewart, 1947; Merbs and Wilson, 1960; Pickering, 1979; Jur- main, 1977; Edynak, 1976; Martin et al., 1979); and there is a great deal of information available on the distribution of lesions in the spine (Stewart, 1947; Anderson? 1963; Merbs, 1969)). The distribution of lesions seen in the AL-288 spine is not common among human popula- tions in our experience; and similar patterns are not reported in the literature of paleopath- ology. AL-288 differs from what we would expect in human osteoarthritis in the distribution of lesions by region, in the balance of proliferative changes under the anterior longitudinal ligament when compared with osteophyte formation? and in the lack of marked changes in the peripheral joints.

Comparative aspects of degenerative joint disease must be considered in any discussion of hominids as remote from modern humans as the australopithecines. In general, large body sue and locomotor patterns are implicated in the distribution and frequency of degenerative joint disease in mammals (Fox, 1939; Harris, 1977; Sokoloff, 1969). While the australopithecines clearly resembled modern humans more than the other living hominoids in their locomotor morphology, they were smaller, and it is not clear that humans


provide the only appropriate model for degenerative joint disease in their spines.

One of us has compared vertebral lesions in humans, gorillas, chimpanzees, orangs, gib- bons, and macaques (DeRousseau et al., 1980). Results pertinent to the present discussion are presented in Table 4. A relatively high frequency of osteoarthritis was observed at the lumbosacral junction in all genera. Lesions at the cervical discs were next most common, and thoracic osteoarthritis least frequently observed. This pattern was most consistent in humans, gorillas, and chimpanzees, who appear to differ only in the distribution of Ium- bar osteoarthritis, the two ape species showing osteoarthritis primarily at the zygapophyseal joints and humans more commonly at the vertebral bodies. The orangutan differs from other great apes in that thoracic disc degeneration is relatively more frequent than cervical osteoarthritis and almost as frequent as the zygapophyseal changes in the lumbar region. A similar trend toward a generalized expression of osteoarthritis characterizes the gibbon and macaque data. Both of these genera show relatively high frequencies of lesions throughout the vertebral column, and no consistent localization at the discs or the zygapophyses. In summary, although several patterns of primate osteoarthritis emerge from these data, none of them show localization of the disease in a single region of the vertebral column.

On the other hand, ventral growth extending beyond the ring epiphyses and presumably occurring after epiphyseal fusion does appear to be localized to the thoracic region in most genera, although in all but chimpanzees and macaques the frequency of Occurrence is very low. The moderate ventral growth of chimpanzees is most frequent in the midthoracic region; and, although macaques show postfusion ventral growth throughout the vertebral column, the highest frequencies of occurrence are likewise in the midthoracic vertebrae. However, no cases of ventral growth were as pronounced as that observed in AL-288.

Clearly, the AL-288 lesions do not mimic in detail any of the primate patterns described above. Although thoracic lesions are observed in most specimens, they generally do not oc- cur without involvement in other parts of the vertebral column. Similarly, postfusion ventral growth in these genera is not as pronounced, nor does it show the same pattern of association with joint disease and disc disease

as that observed in AL-288. Thus, these nonhuman primates fail to provide support for a diagnosis of degenerative joint disease in AL- 288.

A common joint disease of humans that does correspond in many details to the lesions seen in AL-288 is Scheuermann disease or juvenile in kyphosis dorsalis. Scheuermann disease is a relatively common, largely benign condition that begins in adolescence and usually centers on the lower thoracic spine. Disc space is lost, producing a “round back” kyphosis. The disc herniates anteriorly under the anterior longitudinal ligament, beneath the ring epiphysis, or into the vertebral body, producing Schmorl nodes. Healing usually occurs by age 20, the bony defects becoming consolidated. Early fusion of the ring epiphyses is common. Healed lesions are reflected in kyphosis, wedging of vertebral bodies, and loss of disc space (Jaffe, 1972: 621-628; Epstein, 1955: 239-244).

Population studies, most based on routine radiography of military recruits, report an incidence in young adults of 0.4 to 8.3% (Sfirenson, 1964). Early reports stress that frequency is much higher in males than in females, but most of these were based on series of patients treated for back pain or other com- plications of their kyphosis. More recent sur- veys suggest that sex incidence is more nearly equal, and that adolescent boys are more likely to engage in activities that cause the lesions to become symptomatic (Jaffe, 197% Halal et al., 1978; Butler, 1955). The only fully prospec- tive survey of which we are aware uses a random sampling technique and reveals the highest population incidence reported in the literature (15.3%, n = 466). In this same study, 42.6% of a clinical series complaining of back- ache were found to have Scheuermann disease (Stoddard and Osborn, 1979). Sex and age distribution of the sample is not reported.

The etiology of Scheuermann disease is ob- scure. I t is not an osteochondritis, as was orig- inally reported (Bradford and Moe, 1975). An argument has been presented for autosomal dominant inheritance (Halal et al., 1978) based on an analysis of five pedigrees, and other sources have pointed out familial occurrence. A search for abnormalities of bone mainte- nance and calcium metabolism in 12 active cases produced a suite of abnormalities but no single explanatory model (Bradford et al., 1976). The early studies implicated rural resi- dence, farm labor, various athletic activities, and weight lifting in the etiology of the condition (Jaffe, 1972; Epstein, 1955; Scheuermann,

TAB

LE 4

. Fre

quen

cies

ofo

steo

arth

ritis

(OA)

and

pos

tfus

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th in

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mb

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5-7

1-3

4-6

7-9

10-1

2 1-

3 L

4-SI

c)

Gor

illa

8

2-4

5-7

1-3

4-6

7-9

10-1

2 T1

3-L2

L

3-S1

F? 0

Pos

teri

or O

A

0.0

0.0

0.0

0.0

0.0

0.08

0.

17

0.33

0

Ven

tral

gro

wth

0.

08

0.08

0.

08

0.08

0.

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0

Pos

teri

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A

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0.

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17

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0.

33

Ant

erio

r O

A

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0.

04

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tral

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12

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Pan

11

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3 4-

6 7-

9 10

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T13-

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An

teri

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OA

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24

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0.

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21

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An

teri

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OA

0.

17

0.33

0.

17

0.0

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0.

33

0.25

0.

58

"8 8 P

oste

rior

OA

0.09

0.18

0.

03

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0.

03

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0.

55

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p

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tral

gro

wth

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30

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2

Ven

tral

gro

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07

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0.07

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0 s B "C

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tral

gro

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06

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0 0.

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0 *

Mac

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6 2-

4 5-

7 1-

3 4-

6 7-

9 10

-12

1-3

4-6

L7-S

1 3

Post

erio

r OA

0.

22

0.17

0.

28

0.11

0.

17

0.44

0.

17

0.17

0.

58

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An

teri

or

OA

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44

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0.

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11

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0.

17

0.17

0.

17

0.28

a 8

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tral

gro

wth

0.

22

0.61

0.

56

0.94

1.

00

0.56

0.

39

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0.

08

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teri

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A r

efer

s to

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thri

tis o

f th

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gapo

phys

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ior

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to d

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disc

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ease

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h fr

eque

ncy

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alcu

late

d as

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perc

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ge o

f all

the

vert

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l el

emen

ts e

xam

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in a

ny c

ateg

ory

that

exh

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oste

ophy

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nor

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rem

odel

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in q

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In o

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to p

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ughl

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mpa

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a on

eac

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divi

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8 ex

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ophy

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t fe

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tha

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ir v

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joi

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Not

e th

at e

ach

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be

char

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rize

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its

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stri

butio

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5 i

Pos

teri

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A

0.07

0.

13

0.07

0.

07

0.0

0.0

0.13

0.

47

An

teri

or

OA

0.

07

0.07

0.

27

0.13

0.

07

0.27

0.

13

0.27

0

Hyl

obat

es

6 2-

4 5-

7 1-

3 4-

6 7-

9 10

-12

T13-

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3-5

L6-

Sl

0.25

P

oste

rior

OA

0.

28

0.11

0.

11

0.06

0.

0 0.

44

0.17

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17

An

teri

or

OA

0.

17

0.17

0.

39

0.17

0.

33

0.28

0.11

0.33

0.

58

$ z re

mod

elin

g th

roug

h th

e ve

rteb

ral

colu

mn

(see

text

for

det

ails

).

AUSTRALOPI’IFECINE VERTEBRAL PATHOLOGY 99

1977; Wassmann, 1951), and recent studies indicate that traumatic episodes are still an important factor in case-finding (Halal et al., 1978). Comparisons of urban, mining, and farming communities have produced very dif- ferent incidence figures, arguing that activity and occupation are contributing factors (Wass- mann, 1951; Stoddard and Osborn, 1979). Therefore, it seems likely that some model including genetic predisposition, habitual activity, and trauma is most promising.

In a report on surgical findings in two active cases, Bradford and Moe (1975) described the anterior longitudinal ligament as being arranged like a bowstring across the region of maximum curvature overlaying the herniated discs. Anterior growth of affected vertebrae can be marked (Butler, 1955: 898; Fischer and Volk, 1970), resulting in vertebrae that are both longer and wider than normal. In normal individuals, dorsal kyphosis increases with age due to loss of disc space and wedging of the vertebral bodies. These age changes are even more pronounced in Scheuermann disease, the normal pattern of continued growth in vertebral body dimensions being accentuated. Fischer reports vertebral bodies about 0.5 cm longer and wider in individuals with Scheuer- mann disease than in normal individuals throughout adult life (Fon et al., 1980; Fischer and Volk, 1970). An explanation linking kyphosis and this continued apposition under the anterior longitudinal ligament is provided by an experimental model first suggested in Wassmann’s early study (1951). When rat tails are bent and restrained with wire in a bent position, bone forms on the entire longitudinal face on the concave side, and to a limited degree at the margins of the annulus on the convex side (Storey, 1981). The resulting pattern of new bone formation matches that seen in AL-288 in detail and suggests that Scheuer- mann disease is an appropriate diagnosis.

Implications for australopithecine locomotion

Scheuermann disease is most common in thoracic vertebrae 6 through 10, with greatest involvement at 7. The mean number of vertebrae affected is 4.5 (Dameron and Gulledge, 1953). The AL-288 lesions fit this pattern well, but we may ask what functional meaning un- derlies this pattern. The athletic activities that are implicated in causing back pain in Scheuermann disease are very diverse, but weight lifting is mentioned in several ac- counts. Similarly, degenerative joint disease

of the lower thoracic and upper lumbar vertebrae is related to occupational trauma to the spine in adults who lift heavy weights (Ep- stein, 1955: 218). Similarly, fractures of the vertebrae due to acute hyperflexion in convul- sions tend to localize between thoracic vertebrae 3 and 7 (Epstein, 1955: 333-335).

The lesions in the AL-288 spine are most pronounced at the level of thoracic vertebra 8, the point at which the range of motion in the modern human thoracic spine is greatest (Moskowitz, 1979). AL-288 has a marked kyphosis and loss of disc space in this region. This could result, as in the traumatic associations discussed for Scheuemann disease and in vertebral fractures, from lifting heavy ob- jects. However, the similar patterning in con- vulsion injuries suggests an alternate explanation. Compression in the lower thoracic spine might result from using the trunk to lift weight, but pronounced ventral flexion on lifting the body from a fixed arm or arms is equally plausible. We do not mean to suggest that Lucy was a lady weight lifter. However, her spine indicates compression resulting from heavy loading or forceful ventral flexion. Such activities might include movements as diverse as arm-swinging, bridging, crutch-walking, or any climbing activity including forced ventral flexion of the trunk, as well as a whole repertoire of lifting and carrying activities. The heavy musculature in the shoulder and upper trunk suggested by the long cervical spinous processes and robust thoracic neural arches in the other Afar vertebrae support this interpretation, as do the bones of the hand (Tuttle, 1981). Scheuermann dorsal kyphosis secondary to loading of the thoracic spine in lifting, carrying, o r climbing is the most appropriate diagnosis for the lesions in the AL-288 spine.

Was Lucy maladapted to the demands of her behavioral repertoire? The secondary literature in our field is full of statements to the effect that arthritis patterning in modern humans is evidence for incomplete adaptation to upright posture. We feel that such statements represent a misunderstanding of the evolutionary process, because all successful forms can be expected to be well-adapted. Condi- tions such as osteoarthritis or Scheuermann disease that have a traumatic or “wear and tear” component are not maladaptive in an evolutionary sense. They are universal in large-bodied land animals, and are best seen as consequences of size, length of life, and life events in individuals. However, the pattern- i n g of such lesions is of evolutionary interest.


The distribution of lesions in body regions is the result of habitual activity and morphological patterns. The correspondence of Lucy’s lesions to human Scheuermann disease sup- ports a humanlike characterization of the total morphological pattern of the australopithecines, although climbing and acrobatic activities may have been proportionately more important than they are in modern humans.

ACKNOWLEDGMENTS

This research was supported in part by the Research Incentives Program, Indiana Uni- versity, and by the Northwestern University Research Committee. We would like to ex- press our appreciation to M.E. Rutzmoser, Museum of Comparative Zoology, Harvard University, for access to gibbon skeletons in her collections. The aid and hospitality provided by the staff of the Cleveland Museum of Natural History, and especially by W.H. Kim- be1 and B.M. Latimer, were invaluable. Help- ful comments on the manuscript were provided by P.L. Jamison, R.J. Meier, S.G. Knick, R.B. Pickering, and R.H. Tuttle.

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