THE EVOLUTION OF THE HUMAN FOOT, WITH ESPECIAL REFERENCE TO THE JOINTS

By HERBERT ELFTMAN AND JOHN MANTER

Columbia University

THE current divergence of views concerning the evolution of the human foot is due largely to a lack of accurate knowledge concerning the functioning of the ape foot, and a concentration of attention on morphological features less intimately concerned with the action of the foot than arc the joints. By means of an apparatus for studying the instantaneous distribution of pressure in the sole of the foot, we have been able to make an accurate comparison between the method of function of the chimpanzee foot and that of man (Elftman and Manter, 1935). In thel present paper we shall consider especially the joints of the chimpanzee foot in comparison with Man, with regard to their bearing on the evolution of the human foot.
TIlE TRANSVERSE TARSAL JOINT AND THE LONGITUDINAL ARCHI

The transverse tarsal joint (mid-tarsal, Chopart's) lies between the calcaneus and talus on one side and the cuboid and navicular on the other (figs. 1, 3). Movement in this joint allows the forepart of the foot, which is quite rigidly attached to the navicular and cuboid, to move with respect to the calcaneus and talus about an axis which is shown in fig. 2. These movements we shall refer to as plantar-flexion and dorsi-flcxion about the transverse tarsal joint. Since the axis of the joint in the normal position of the human foot is inclined at a considerable angle to the horizontal, plantar-flexion with the calcaneus held imnmovable results in abduction of the forepart of the foot. Dorsi-flexion results in abduction. When movement takes place in the transverse tarsal joint with the foot on the ground, the tuber calcis and the anterior part of the foot must remain in contact with the substratum. Under these circumstances dorsi-flexion about the transverse tarsal joint results, not in abduction of the forepart of the foot, but in a lowering of the joint and a flattening of the foot. In the chimpanzee the transverse tarsal joint is freely movable, while in the human foot with a well-developed longitudinal arch the joint is relatively immobile. The human foot with its longitudinal arch (fig. 1B) displays the same relationships between the forepart of the foot and the calcaneus and talus that we find in the chimpanzee foot when it is plantar-flexed about the transverse tarsal joint (fig. 1A). We are justified in concluding that in the human foot the transverse tarsal joint has become fixed in a plh.ntar-flexed position.

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57

Additional evidence for this concept is to be found in the prevalence of mobility in the transverse tarsal joint in flat-footed humans. It seems likely that mobility in the transverse tarsal joint, rather than being a result of flat-footedness, is more often a cause.

T T JOINT,
A

,w

Fig. 1. Chimpanzee and human feet in medial view. A, chimpanzee foot in an arboreal position; plantar-flexion about the transverse tarsal joint. B, human foot on the ground. C, chimpanzee foot on the ground: pronation with dorsi-flexion about the transverse tarsal joint. T.T. transverse tarsal joint.

The evolution of the longitudinal arch in Man is consequently due to an immobilization of the transverse tarsal joint in a plantar-flexed position. To provide a more complete explanation involves the determination of the

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Herbert Elftman and John Manter

mechanism of immobilization. This cannot be done at present. It might be due to a shortening of such connective structures as the plantar aponeurosis, the long plantar ligament and the plantar calcanco-navicular ligament. It could also be accounted for by changes in muscle action. It will be impossible to decide this issue until we are able to settle by experiment the question as to whether ligaments or muscles determine the limits of movement in the joints. The position of the axis of the transverse tarsal joint which we have determined differs from the position given by Fick (1911). There can be no doubt concerning the position of the axis in the chimpanzee. Since our determinations on mobile and juvenile human feet agree with the results in the chimpanzee, we feel that Fick must have been misled by movements in other parts of the foot than the transverse tarsal joint.

T 2

U~~~~~
Fig. 2. Chimpanzee and human feet in dorsal view. A, chimpanzee foot on the ground. B, human foot on the ground. C, chimpanzee foot plantar-flexed about the transverse tarsal joint, as in fig. 1 A. T. axis of transverse tarsal joint. U. axis of upper ankle joint. L. axis of lower ankle

joint.

The importance of plantar-flexion or inversion about the transverse tarsal joint as one of the factors in the evolution of the longitudinal arch has already been stressed by Keith (1923, 1929). The extension of his theory so as to assign prime importance to the tibialis anterior as an invertor of the foot has, however, been rendered doubtful by the studies of Fick (1911, 1931) and by our own determination of the position of the axis of the transverse tarsal joint. The tibialis anterior may well be a postural muscle, intimately correlated with the evolution of the upright posture of man, due to its action about the upper ankle joint. Attempts have been made to explain the evolution of the longitudinal arch on the basis of changes in the position of the talus. It is true that plantar-

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59

flexion in the transverse tarsal joint, with the heel and anterior support of the foot in contact with the ground, does tend to bring the talar head more directly above the calcaneus, especially since this plantar-flexion is usually associated with inversion about the lower ankle joint. But the change in position of the talar head is a consequence, not a cause, of longitudinal arch production. The arch is a subtalar structure, depending on the relationship of the calcaneus to the anterior part of the foot. Weidenreich (1921) recognises that plantar-flexion about the transverse tarsal joint has occurred in the evolution of the longitudinal arch, but considers this as being subsidiary and subsequent to the upward inclination of the calcaneus. It seems obvious to us that the upward inclination of the calcaneus is a necessary concomitant of fixation of the transverse tarsal joint in the plantarflexed position and cannot be considered as a cause of the plantar-flexion. Certainly Weidenreich's argument that in Man the weight of the body is concentrated on the calcaneus and thus is responsible for its tilt is not substantiated by our researches on the path of the resultant of pressure in the foot (Elftman and Manter, 1935). In the chimpanzee the resultant lingers for a longer time in the tarsal region than it does in Man, but the chimpanzee gives no evidence of a calcaneal tilt. Recognition of the evolution of the longitudinal arch as having been due to plantar-flexion about the transverse tarsal joint serves also to explain the fact that in the human foot the metatarsals are in line with the long axis of the calcaneus, while in the ape foot, as seen resting on the ground (fig. 2A), the metatarsals diverge laterally from the long axis of the calcaneus. If the chimpanzee foot is plantar-flexed about the transverse tarsal joint, with the heel and anterior support of the foot still in contact with the ground (fig. 2 C), it will be found that the metatarsals in their new position are parallel to the long axis of the calcaneus.
THE LOWER ANKLE JOINT

In the ankle there are two joints about which movement is possible. In the upper ankle joint (talo-crural), the tibia can rotate backwards or forwards over the trochlea of the talus. It is the lower ankle joint (subtalar), however, to which we shall first direct our attention. In this joint the articulation is between the'talus on one side and the calcaneus, cuboid and navicular on the other. This gives rise, according to the usual description, to the possibility of gliding movements in the joint. A more illuminating concept is that of Donitz, modified by Fick (1911), who demonstrated that, in spite of the bewildering congeries of articular surfaces involved, the movement in the lower ankle joint can be quite accurately described as rotation of the entire subtalar portion of the foot about a line, the compromise axis of the lower ankle joint. The position of this axis is shown in figs. 2, 3, 4 and 5. When looking at the right foot from in front, a clockwise rotation of the foot about this axis would give rise to eversion, a counter-clockwise rotation to inversion. It is possible to tell whether a foot is being held in an inverted or everted

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Herbert Elftman and John Manter

position by noting the relations of the talus to the calcaneus, since the joint surface passes between these bones. The talus and calcaneus of the chimpanzee are represented in fig. 3A in the relative positions they occupy when on the ground, but with the calcaneus tilted so as to make comparison with the other figures easier. Fig. 3C shows these bones in the positions they occupy in the arboreal position of fig. 1 A. It is obvious that when on the ground the chimpanzee foot is everted about the lower ankle joint, while in the arboreal position illustrated a moderate degree of inversion is present. If the human relationships (fig. 3B) are now compared with the two figures of the chimpanzee, it is apparent that the usual human position in standing resembles that of the chimpanzee when moderately inverted.

Fig. 3. Anterior view of the talus and calcaneus, with the plane determined by the axes of the transverse tarsal and lower ankle joints perpendicular to the plane of the figure. A, chimpanzee, showing the relationships of the bones in the terrestrial position of fig. I C, but with the whole figure rotated outward so as to bring the calcaneus into a position congruent with that of fig. 3 C. B. human. C, chimpanzee, plantar-flexedl about the transverse tarsal joint with accompanying inversion about the lower ankle joint, as in fig. 1A. U. axis of upper ankle joint. T., L. axes of transverse tarsal and lower ankle joint. A.L.P. antero-lateral process, its extent roughly indicated by the dotted line.

The normal human foot can never achieve as highly everted a position as that shown to be the common terrestrial position of the chimpanzee. One of the reasons for this is found by an inspection Of the anterior portion of the calcaneus of Man. Both in the anterior and lateral views of fig. 5, and in fig. 3 B. there can be seen Pa bony process, which we shall call the antero-lateral process of, the calc-aneus, which prevents extensive movements of eversion of the talus with respect to the calcaneus. No indication of this process can be found in the calcaneus of either chimpanzee or gorilla. It furnishes one of the most easily recognizable diagnostic cllaraclteristics of the human type of
calcaneuls.
RELATIONSHIP OF THE AX~ES OF TIDE TRANSVERSETARSAL ANC LOWER ANKLE JOINTS The articulation between the talus and the navicular presents a peculiar

problem, since movement in this articulation may take place either about the about e axis of the transverse tarsal joint, or axis of tigelower ankle joint,tcp

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61

about both axes simultaneously. This would not be possible if the articular surface were not essentially spherical, with the two axes mentioned intersecting at the centre of curvature of the sphere. Since the two axes do intersect at this centre of curvature, free movement can take place simultaneously in the lower ankle joint and in the transverse tarsal joint. The extent of the articular surface on the head of the talus is intimately correlated with the degree of movement possible. The greater range of eversion possible in the chimpanzee is correlated with the extension of the articular surface (fig. 4) further posteriorly on the lateral side in the chimpanzee than in Man.
THlE UPPER' ANKLE JOINT

The talo-crural or upper ankle joint allows movement between the tibia and fibula, acting together, on one side, and the talus on the other. We should consequently expect that in the evolution of the human upright posture, with the knees held near the midplane of the body during movement, there would be a remodelling of the tibia, fibula and talus. The differences between the chimpanzee and Man in the tibia and fibula have been adequately treated by former investigators. A comparison of the talus of Man with that of the chimpanzee shows that the troclhlea in the human has been rotated upon the body of the talus. This rotation is clearly seen in the dorsal views of the bones (fig. 4) by concentrating attention upon the angle between the neck of the talus and the axis of the upper ankle joint. This angle is larger in Man than in the chimpanzee. This difference in angle has been noted by many previous workers. They, however, have interpreted it as indicating a shift in position of the neck of the talus. That the neck has not changed can be seen by noting its relations to the articular surfaces as seen in ventral view. Further confirmation of our interpretation that it is the trochlea which has undergone rotation emerges from a comparison, in posterior view, of the relation of the trochlea to the posterior calcancal articular surface. The medial border of the trochlea is higher in Man than in the chimpanzee, as can be seen in the anterior and posterior views (fig. 4). This is also correlated with changes in the tibia.
TIHE METATARSO-PIIALANGE'AL JOINTS

That the five metatarso-phalangeal joints are differently oriented in MIan than in the chimpanzee and gorilla has been noted by many investigators, including Morton (1922) and Weidenreich (1921). In fig. 6 the heads of the metatarsals are shown in projection upon a vertical plane. It is apparent that in the human there is not a well-developed transverse arch in this region, as there is in the chimpanzee. In a previous paper (Elftman, 1934) the fact that there is no concentration of pressure, such as one would expect at the ends of a functional arch, was taken to be an indication of a lack of a transverse arch functional in weight-bearing in this region of the human foot. It is possible for

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Herbert Elftman and John Manter

the human foot to distribute its pressure over this entire region of the ball of the foot when the heel is lifted, because of the disposition of the axes of the five metatarso-phalangeal joints. In the chimpanzee this is not possible. The axes of the fifth and first metatarso-phalangeal joints are sharply inclined to the ground. It is consequently impossible for the foot as a whole to bend in a vertical direction in this region. When the heel of the chimpanzee and then the transverse tarsal joint are lifted, pressure is transferred not to the region of the metatarsal heads but to the toes. The evolutionary changes which have resulted in the human condition have been described as torsions of the metatarsals, the first in one direction, the four lateral ones in the other. It is unquestioned that the distal portions of the metatarsals have undergone changes in which the bases have not participated.
THE JOINT AT THE BASE OF THE FIRST METATARSAL

The opposability of the hallux in the apes contrasts greatly with its permanently adducted position in Man. Since this condition is apparent externally it has been seized upon as the prime difference between the ape and the human foot. There is no doubt but that in the evolution of the foot other features are more important, but it is true that an adducted hallux provides a stronger anterior pillar for the longitudinal arch than would an abducted hallux. The articular surface on the first cuneiform of the chimpanzee is strongly convex and faces medially. In Man the articular surface is more nearly flat and faces more anteriorly. Some specimens of human cuneiform do, however, possess a markedly convex surface, the axis of curvature being oriented as in the chimpanzee, but the articular surface faces forward. There is no doubt whatever that the human condition could have evolved from that found in the apes. Detailed evidence for this has been put forward by Schultz (1930).
THE BONES OF THE FOOT

The evolutionary changes in the joints have inevitably been accompanied by changes in the bony elements. It is advisable, therefore, to compare briefly the more essential features of the bones of the human and chimpanzee feet.

The talus In comparing the talus of Man with that of the chimpanzee it is necessary that the two bones be oriented in similar fashion. The usual method is to use the trochlea as a basis of orientation. This is highly unfortunate, since we have seen that the trochlea changes in the course of evolution. We shall therefore orient the two bones with the axes of the lower ankle joints parallel and the ventral articular surfaces in congruent positions. When this is done, many of the differences which have been described as existing between the two bones are seen to be due to faulty orientation. The general similarity of the ventral articular surfaces (fig. 4) is apparent. It is true that the radius of curvature of these surfaces is shorter in the chimpanzee than

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in Man. There is difficulty in estimating the importance of this, however, since the radius of curvature of these surfaces is shorter in small human feet than in large ones. The rotation of the trochlea with respect to the rest of the bone and the increased height of the medial border of the trochlea in Man have already been discussed. The latter feature is of importance in studying the head of the talus. In the anterior view of fig. 4, it is noticeable that the greatest length of the talar head in the human makes a larger angle with the dorsal surface of the trochlea than it does in the chimpanzee. This has been interpreted as due to a torsion of the talar head. It is obvious, however, that here, again, it is the trochlea and not the head of the talus that has changed. The difference in

k~~~~~~~~~~
71
_

u,

X.

DORSAL

VENTPRAL

ANTERIOR

POSTER/OR

Fig. 4. The talus of man and chimpanzee oriented with the axes of the lower ankle joints parallel. Upper row: chimpanzee. Lower row: human. U. axis of upper ankle joint. L. axis of lower ankle joint.

extent of articular surface on the head of the talus when the chimpanzee is compared with Man contributes to this apparent torsion. But this we have already found to be due to greater possibilities of eversion in the chimpanzee, not to a change in the axis of the joint. The variations in the anterior extent of the trochlear surface in primitive tribes of Man have been extensively discussed by anthropologists and need not be considered here. The calcaneus When the calcaneus is oriented by means of the axes of the lower ankle joint and the transverse tarsal joint (fig. 5), there is a striking similarity between the chimpanzee and human bones. One of the chief differences to be noted is the appearance in Man of a new process, the antero-lateral process of the calcaneus, which may be seen in anterior, lateral and dorsal views. The significance of this in limiting eversion in the lower ankle joint has been mentioned.

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Herbert Elftman and John Manter

The similarity in contour of the facets for articulation with the cuboid is worthy of mention. Except for the additional area due to the antero-latcral process, the human facet illustrated is characteristically like that of the chimpanzee. In some other human calcanei examined, the transverse groove which indents this facet is not so well developed. It is likely that variations in this groove arc correlated with the variability in the mobility of the transverse tarsal

joint.
The shape of the tuber calcanci, seen in posterior view (fig. 5), is extremely variable in Man. It is frequently quadrate in appearance, but varies from this condition to one of ovate contour resembling more closely the chimpanzee. The calcaneus of Man is relatively longer and stouter than that of the chimpanzee. In this character the gorilla resembles Man more closely.

I -

(~~~~~~~~~~~~~~~~~D

"9'

-.ALP~~~~Y XLj.4P'~t
9\ X

-ALPAL

DORSAL

V <'tEV
L A TERAL

AN TER/IOR

~ ~ ~ ~ ~ ~ ~\A \\
FOSTERiOR

Fig. 5. The calcaneus of Man and chimpanzee oriented with the axes of the lower ankle joint parallel. Upper row: chimpanzee. Lower row: human. L. axis of lower ankle joint. T. axis of transverse tarsal joint. A.L.P. antero-lateral process of calcaneus.

The sustentaculum tali has received the attention of previous investigators, some of whom have felt that its position in the human required extensive explanation. A study of the anterior and posterior views of fig. 5 reveals no significant difference in the relationship of the sustentaculum to the rest of the calcaneus between the chimpanzee and Man. Whatever differences it has with respect to the substratum as the foot is used must be due to the position of the entire calcaneus, not to any change in the sustentaculum alone. The trochlear process or peroneal tubercle is exceedingly variable in Man. In the chimpanzee illustrated this process is more highly developed than it is in the human, but in another specimen of chimpanzee calcaneus it approaches closer to the human condition.

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Other tarsal elements The navicular, cuboid and second and third cuneiforms of Man are longer than those of the chimpanzee, when compared with the combined length of tarsus and metatarsus. This lengthening is balanced to a certain extent by the shortening of the four lateral metatarsals. The euboid of Man has a larger surface for articulation with the calcaneus, covering in part the anterior face of the antero-lateral process of the calcaneus. The differences in relative proportions of the second and third cuneiforms cannot be discussed here; they may be correlated with a more important feature, the shape of the first cuneiform. The surface on the first cuneiform which articulates with the first metatarsal has already been discussed.

Fig. 6. The heads and the articular surfaces of the bases of the metatarsals, projected upon a vertical plane. The articular surfaces of the bases are shown in dotted lines. A, human. B, chimpanzee in normal terrestrial position. C, chimpanzee with foot plantar-flexed about the transverse tarsal joint.

Metatarsals and phalanges In addition to the torsion of the heads of the metatarsals with respect to their bases, there is another difference of importance between Man and the chimpanzee. This is the shortness of the four lateral metatarsals and their phalangeal series in the human. Schultz (1930) has demonstrated that in the course of evolution the first metatarsal and its phalanges have undergone no marked change in length, when measured with relation to the rest of the foot, but that there has been an actual reduction of the four lateral metatarsals and their phalanges, especially the second phalanges. It is significant that in the gorilla, which is more terrestrial in its habitat than is the chimpanzee, the lateral phalanges are shorter.
THE MECHANISM OF FOOT EVOLUTION

The contribution of the present paper lies chiefly in a clarification of the structural differences between the ape foot and the human. An analysis of the mechanism of foot evolution must interpret these structural differences from two points of view: first, the changes in the developmental process which lead
Anatomy LXX
5

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Herbert Elftman and John -Manter

to differences in adult structure; and secondly, the differences in function of the adult structures which determine whether they shall be judged fit or unfit by the environment in which they struggle for existence. The first of these problems has been studied by numerous investigators, notably in recent years by Straus (1927). It would be well worth while to reanalyse the descriptive embryological data available in terms of the structural changes noted in the present paper, with a view to finding, not evidence for recapitulation, but some clue to the developmental factors involved. We fully realise that an analysis into such factors as differential growth rates is but a preliminary step toward a definitiv-e analysis in more fundamental terms, such as genie differences. The second problem, that of selection by the environment for procreation of those structures which are functionally advantageous, is in some ways more easily studied. We can determine, in a fashion, the changes which have taken place in the environment. In the case at hand, we at least know the environments in which the chimpanzee and Man live. We can tell, by studying the structures experimentally, why they have survival value in the forms now living. If we knew more definitely the environments which surrounded the stages intervening between the ape ancestor and Man, we could make a fair estimate as to which types of structure would have had survival value during this

critical period.
SUMMARY

The fundamental similarity in architecture demonstrated in the comparison of the foot of the chimpanzee with that of Man leaves no doubt as to the evolution of the human foot from that of an ape. But superimposed upon this fundamental similarity are important differences which allow us to make the following list of the most important changes which the foot has undergone in its evolution from ape to Man: 1. Stabilisation of the transverse tarsal joint in a position of plantarflexion. This accounts for the longitudinal arch and partially for the alignment of the lateral metatarsals with the long axis of the calcaneus. 2. Prevention of extensive eversion in the lower ankle joint, partly by the appearance of a new process, the antero-lateral process of the calcaneus. 3. Rotation of the trochlea of the talus with respect to the body of the bone, and raising of the medial border of the trochlea, correlated with the changed position of the tibia in upright locomotion. 4. Torsion of the metatarsal heads, allowing flexion in the metatarsophalangeal joints perpendicular to the ground. This eliminates the anterior transverse arch as a functional factor and allows the distribution of pressure over the ball of the foot. 5. Permanent adduction of the hallux, forming a strong anterior support for the longitudinal arch. 6. The following changes in proportion: shortening of the four lateral metatarsals and their phalangeal series; increase in relative length of the

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cuboid, navicular and first and second cuneiforms; and increase in stoutness and length of the calcaneus. Although the gorilla resembles Man more closely than does the chimpanzee in the relative shortness of the lateral digits, it shows no indication of the more fundamental changes, such as those in the transverse tarsal joint, which are essential for the development of the human condition. The fact that the human foot, adapted as it is for walking on the ground, bears a closer resemblance to the ape foot as used in arboreal than in terrestrial locomotion may be regarded as another evidence of Man's arboreal ancestry. It would also suggest that the essential features of Man's foot were acquired at an early stage of his terrestrial existence, rather than after long apprenticeship on the ground. It would be perfectly possible, however, for a human type of foot to evolve from either the chimpanzee or gorilla foot as now constituted, since the structures which, by modification, can give rise to the human structure, are still intact.
REFERENCES ELFTMAN, H. (1934). "A cinematic study of the distribution of pressure in the human foot." Anat. Rec. vol. LIX, pp. 481-91. ELFTMAN, H. and MANTER, J. T. (1934). "The axis of the human foot." Science, vol. LXXX, p. 484. (1935). "Chimpanzee and human feet in bipedal walking." Amer. J. phys. Anthrop. vol. xx, pp. 69-79. FICK, R. (1911). Handbuch der Anatomie und Mechanik der Gelenke. Dritter Teil. Jena: Gustav Fischer. (1931). "tber die Bewegungen und die Muskelarbeit an den Sprunggelenken des Menschen." S.B. preuss. Akad. Wis8. S. 458-94. KEITH, A. (1923). "Man's posture." Brit. med. J. pp. 669-72. (1929). " The history of the human foot and its bearing on orthopedic practice." J. Bone Jt Surg. vol. XI, pp. 10-32. MORTON, D. J. (1922). "Evolution of the human foot. Pt. I." Amer. J. phys. Anthrop. vol. v, pp. 305-36. SCHULTZ, A. (1930). "The skeleton of the trunk and limbs of higher primates." Hum. Biol. vol. II, pp. 303-438. STRAUS, W. L., Jr. (1927). "The growth of the human foot and its evolutionary significance." Contr. Embryol. Carneg. Instn, vol. XIX, pub. 380, pp. 93-134. WEIDENREICH, F. (1921). "Der Menschenfusz." Z. Morph. Anthr. Bd. XXII, S. 51-282.

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