Development of the Human Hind Limb and itsImportance for the Evolution of BipedalismCHRISTINE TARDIEU

In fossil hominins we must reconstruct behavior, including locomotion, largelyfrom preserved skeletal features. The interpretation of such features has beencontroversial in some cases because we do not understand their true functionalsignificance. One way to explore this issue is to examine both normal andabnormal modern human growth in clinical cases to see what affects the loco-motor skeleton and what appears to be of genetic and epigenetic origin. Theseresults can then be used to interpret fossils.

For example, while learning to standand walk, the infant progressivelystraightens its skeleton and modifies itdrastically. This raises the question ofwhich features of the human lowerlimb arise postnatally and how? Here Ireview the growth of the lower limbfrom newborn to adult in associationwith gait acquisition. The growth phe-nomena described here are essentiallypostnatal. However, some importantelements of prenatal growth will beconsidered as well.

FORMATION OF THEDIRECTIONAL AXES OF THELOWER LIMBS: ANGULARMODIFICATIONS OFTHE FEMUR AND TIBIA

Gravity is the major influence act-ing on the skeletal modifications that

occur during growth, particularlyduring standing and gait acquisition.In children, the stages of the progres-sive control of balance coordinationof the lower limbs are as follows:1 At6–8 months of age, the infant sitswithout support. At 9 months, itstands erect with a straight trunk. At9–10 months, it gets up while hold-ing onto a support. At 11 months theinfant walks if helped by two hands.At 12 months, it walks if helped byone hand. At 13–14 months, it walksby itself. At 21 months, it walks onirregular surfaces. At 2 years of age,it runs. At 4 years, it can climb astaircase and, at 5 years, can coordi-nate its lower limbs and jump rope.

One of the most striking changesduring gait acquisition, which is visibleto the naked eye, is the reorientationof the tibio-femoral angle (Fig. 1).2

This angle between the axes of thefemoral and tibial diaphyses changesin the loading of the lower limb froma varus (abducted kneejoints) to avalgus (adducted kneejoints) posi-tion. At birth, the lower limbsassume a marked varus position,with abduction of the thigh andadduction of the legs. As the childbegins to stand and walk, the tibio-femoral angle decreases, passing 08between 1.5 and 2 years, then reach-ing a peak valgus position of about108 around 3 years, only to decreaseto a relatively constant angle ofapproximately 68 by 6–7 years of age.This change in hindlimb angulation

is brought about by several separatemodifications of the bones involved,the femur and the tibia.To understand the abilities of our

skeleton to change during growth,we must keep in mind the nature ofthe skeleton of a newborn. The new-born skeleton is largely cartilaginous,with only partial ossification (Fig. 2).The femoral and tibial diaphyses areossified, but the epiphyses are com-prised entirely of cartilage. A nucleusof ossification, which appears on thedistal femoral epiphysis at birth, isgradually replaced by bone via theprocess of endochondral ossification.The bones will be mature when theepiphyseal plates are completelyclosed at the end of the growthphase. The malleability of the neona-tal and infant skeleton, made possi-ble by this important cartilaginouscomponent, is an essential featurefor understanding its development.How does longitudinal growth of

long bones of the lower limb takeplace?3–5 At birth, the lower limbsrepresent 23% of their adult length;at 1 year of age they represent 35%and, at 10 years, 77%. The femurmeasures about 9 cm at birth, but atthe end of growth has elongated five-fold to about 45 cm. Similarly, thetibia measures 7 cm at birth and 35cm at the end of limb growth. Thecontribution of the growth cartilagesis very different. The proximal femurprovides 30% of the femoral length,the distal femur 70%. The proximaltibia provides 60% of the tibiallength, the distal tibia 40%. The kneejoint itself comprises 65% of thelength of the lower limb.Figure 3 presents an overview of

the main angular features thatchange during growth of the femurand tibia: the femoral bicondylarangle, the collo-diaphyseal angle

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Christine Tardieu is a researcher with the‘‘Functional Diversity and Adaptation’’group at the French National Center forScientific Research (CNRS). Her labora-tory (UMR 7179) is located in theNational Museum of Natural History inParis. Her work focuses on comparativeanatomy, functional morphology, evolu-tion, and paleontology of the primatepostcranial skeleton. E-mail: tardieu@mnhn.fr

VVC 2010 Wiley-Liss, Inc.DOI 10.1002/evan.20276Published online in Wiley Online Library(wileyonlinelibrary.com).

Evolutionary Anthropology 19:174–186 (2010)

(neck-shaft angle), the anteversionangle of the femoral neck, and thetorsion of the tibia. The magnitudes

of these parameters will determinethe directional axes of the lowerlimbs in adults.

The Angle of Obliquity of theFemoral Diaphysis

As noted, one of the most distinctivefeatures of the hominid lower limb,which is normally associated with theadoption of bipedal locomotion, is thepresence of an adduction of the kneejoint (genu valgus) and its associatedskeletal feature, the angle of femoralobliquity or bicondylar angle, withsample means around 8–118.

This elevated bicondylar angle is aconsequence of the need to maintainan essentially horizontal plane of theknee joint, as well as flexion andextension of the knee in the parasagit-tal plane. This angle also positions theknee close to the body’s center of grav-ity while in a bipedal striding gait, de-spite a large interacetabular distance.The degree of this angle is correlatedwith the length of this distance.6–10

Figure 4A shows the change of thisangle during infancy. The bicondylarangle is 08 before and immediatelyafter birth. A clear change in angle

appears during the second year oflife. The angle continues to develop,reaching low adult values by thefourth or fifth year after birth. Thistemporal change of the bicondylarangle closely parallels the acquisitionof walking in young children. Indeed,there is little loading of the limbs ina bipedal posture before the firstyear after birth and little loading ofthe knee in a valgus position untilabout two years after birth. The childis then actively bipedal and main-tains the leg in a complete and evenexaggerated valgus position.11–14 Thebicondylar angle of the femur reachesclose to its final value around the ageof eight years, shortly after stabiliza-tion of the tibiofemoral angle.Such a postural and locomotor

connection to the bicondylar angledevelopment has to occur throughthe differential mediolateral meta-physeal apposition at the distal endof the femoral diaphysis during lon-gitudinal femoral growth, with anadditional medial metaphyseal appo-sition.15 Tardieu16 showed a simulta-neous change on the lateral side ofthe distal metaphysis and suggesteda necessary compensation in termsof stability of the joint. The longitu-dinal modeling of the diaphysis bythe angle of obliquity is associatedwith a greater anteroposterior deepen-

Figure 1. Evolution of the tibio-femoral angle from birth to 7–13 years of age (fromSalenius and Vankka2). [Color figure can be viewed in the online issue, which is available atwileyonlinelibrary.com.]

Figure 3. Adult skeleton showing the stud-ied angular parameters. Two are frontal:the femoral obliquity angle and the collo-diaphyseal angle, shown on the right sideof the body. Two are horizontal: antever-sion of the femoral neck and tibial torsion,shown on the left side. [Color figure canbe viewed in the online issue, which isavailable at wileyonlinelibrary.com.]

Figure 2. Radiograph of a newborn’s skele-ton showing both the cartilaginous andthe ossified skeletal segments.

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ing of the lateral side of the metaphy-sis. In nonwalking children, we canshow that the femoral obliquity angledoes not develop (Fig. 4B).13,14,16 Onechild with a spastic diplegy was non-ambulatory until the age of 6 years, atwhich time he underwent rehabilita-tion that allowed him to stand andwalk. At 7 years of age, his bicondylarangle was 1.58. By the age of 10 years,when he was able to move with an or-

thopedic walker two hours a day, thebicondylar angle had reached 58.

In modern humans, the femoralbicondylar angle appears to be an epi-genetic functional trait that developsduring growth in early childhood andis related to the acquisition of erectposture and the onset of walking. Itdoes not develop in nonwalking chil-dren; however it is present in all aus-tralopithecines, suggesting that in

early hominins, as in modern humans,it developed following a change ininfant locomotor behavior. Australopi-thecine infants practiced adductedknee bipedal walking with such fre-quency that a high bicondylar anglelikely emerged early in development.Previous genetic modifications of aus-tralopithecine pelvic shape, particularlythe approximation of the ilio-sacraland hip joints and a large interacetabu-

Box 1. Comparison with Nonhuman Primates and Fossil Hominids

Complex or simple fitting of thediaphysis into the epiphysis:

In both humans and great apes,

the femur of a newborn presents a

flat, regular contact surface at the

distal end of the diaphysis.14,16–18

In humans, the infradiaphyseal

plane remains flat. In contrast, very

early in the development of nonhu-

man primates it is divided by two

grooves, each corresponding to a

crest on the distal epiphysis (Fig.

5). The epiphysis fits tightly into

the diaphysis. The simplification of

the profile of the femoral distal epi-

physeal surface in humans is

opposed to the more complex epi-

physeal profile in great apes.

Because we have also observed this

complex profile in all studied catar-

rhine and platyrrhine primates, this

feature can be considered to be the

general primitive condition com-

mon to nonhominid primates. We

suggest that a more complex fitting

is required to prevent epiphyseal

separation in the context of an ar-

boreal mode of life. The simplifica-

tion of the epiphyseal fitting in

humans may be related to the less

variable postures of the hind limb

in relation to gravity, which leads

to the action of joint forces in a sin-

gle direction.The two juvenile femoral diaphy-

ses attributed to Australopithecusafarensis (AL 333-110 and AL333-111)18 are sufficiently well pre-served distally. They have an infra-diaphyseal plane similar to thatseen in humans (Fig. 6B). Thus,three millions years ago, the convo-luted insertion of the diaphysis into

the epiphysis had already evolvedinto the simplified form typical ofhumans. We can hypothesize thatthe angular remodeling of the fe-mur would have appeared at aboutthe same time as the tight fitting ofthe epiphysis into the diaphysis dis-appeared. It would be interesting totest this hypothesis further and toundertake comparisons withinquadrupedal primates that mightdiffer in predominant loadingregimes (for example, ‘‘terrestrial’’baboons or patas monkeys versusmore arboreal cercopithecines).

The femoral bicondylar angle ingreat apesSome authors argue that the fe-

mur of some nonhuman primatesexhibits a femoral bicondylarangle,19,20 as seen in orang-utans(reaching 68). We have shown thatthe greater height of the medialcondyle in comparison to the lat-eral condyle is the reason for thehigh obliquity angle found in someadult great apes (Fig. 6C), while inhumans the two femoral condylesof subequal height play no part infemoral obliquity.17 In nonhumanprimates, this angle is an epiphy-seal phenomenon. The comparisonbetween human femora and femoraof great apes clearly shows that theangular remodeling of the femur,exclusively diaphyseal and specificto humans, is never present in thegreat apes.18

Genetic limitation on the forma-tion of epigenetic featuresIn Japanese macaques trained for

bipedalism during infancy, lumbar

curvature increases.21 However, thefemoral diaphysis remains straight.The shape of the pelvis in maca-ques is very different; the interace-tabular distance is shorter and thedistal epiphyseal suture of thefemur is deepened. This observa-tion illustrates the genetic limita-tion on the formation of epigeneticfeatures.

Figure 5. A. Adult femur of a chimpanzeeand a human in anterior view. Inferiorbox: Infradiaphyseal plane of two suba-dult femurs. Note the deep grooves in thechimpanzee and the flat surface in thehuman. B. Diaphysis of the fossil AL 333-111 with its flat infradiaphyseal plane. C.Left and right femora of a subadultorang-utan in anterior and posterior views.If the anterior femora mimic an angle ofobliquity, the posterior femurs reveal thatthe diaphyses are straight. [Color figurecan be viewed in the online issue, whichis available at wileyonlinelibrary.com.]

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lar distance, were necessary to promotethis epigenetic feature.

The Neck-Shaft Angle of theFemur

In fetuses and newborns, a definedfemoral neck is absent. Between 3and 6 months of age, the proximalgrowth epiphysis is divided into twoparts, a medial short head part perpen-dicular to the neck axis and a long lat-eral trochanteric part in line with theneck (Fig. 6A).22 Based on Harris’ lines,comparative studies of the growth ratesof these two growth plates show thatthe head growth plate grows 1.6 timesfaster than does the trochanter growthplate (Fig. 6B).15

During growth, the neck-shaftangle decreases. Based on a sampleincluding 74 observations on 23 chil-dren between birth and 17 years ofage, the head-neck angle decreasesfrom 1638 to 1268.18 In one boybetween 2 and 12 years, it decreasedfrom 1548 to 1448. Other data show amean decrease from 1458 to 1258from birth to adulthood.25 In non-

walking children the head-neck angledoes not change (Fig. 4B). Progressivecoxa valga, a progressive increase inthe head-neck angle, appears afterchildhood excision of the hip abductormuscles.24 Closure and opening of theneck angle are related to the samemechanisms of differential metaphy-seal apposition as those described forthe obliquity angle of the femoral dia-physis.15

Radiologic studies show that theangulation of the head growth plate inrelation to the horizontal planeincreases steadily during growth, from118 to 238, while the angulation of thegreater trochanteric apophyseal growthplate remains nearly constant (Fig.6C).23 The constancy of this latterangle is contradictory to the decreasein the cervico-shaft angle duringgrowth. Since this trochanteric anglehas never been measured in associa-tion with the angle of femoral obliq-uity, which is deeply involved in thisosseous remodeling, the questionremains open. It is currently underinvestigation by means of the simulta-neous measurement of the four femo-ral angles (the obliquity angle, cervico-

diaphyseal angle, angle of the trochan-teric growth plate, and angle of thecapital growth plate), on a sample oflongitudinal radiographs.

Anteversion of the Femoral Neck

Anteversion of the femoral neck orfemoral antetorsion describes the an-terior rotation of the proximal end ofthe femur relative to the distal con-dyles (Figs. 3 and 8).

Increase of the femoral

anteversion in utero

An analysis of the intrauterine con-straints linked to the limited extensionof the maternal abdominal cavity is inprogress in our laboratory. Skeletalmodifications of the fetus, such as theincrease in anteversion, could belinked to the obligate hyperflexion ofthe lower limbs on the pelvis. Thishyperflexion of the hip and kneewould be responsible for the creationof a first-order lever (Fig. 7), whichresults in femoral anteversion.26

Postnatal decrease of the femoral

antetorsion

The femoral neck anteversion angledecreases during postnatal growth.Its value ranges between 358–408 innewborns and reaches an averagevalue of 108 in adults.27–31 Moreover,femoral anteversion is higher infemales. It is worth noting the oppositedirection of growth in the anteversionangle during ontogeny, first increasingduring prenatal growth and subse-quently decreasing during postnatalgrowth. Presumably, this reflects differ-ent constraining factors, including spacein the uterus and, postnataly, gravityand the mechanics of bipedalism.The shape of the femoral neck is

mainly determined by the combinedgrowth of the head epiphyseal plateand the greater trochanteric apophy-seal plate. Fabeck33 provided a theo-retical study of the decrease in fem-oral anteversion during growth.

Lateral Tibial Torsion

Similar torsion of the tibia occursaround the longitudinal axis of itsshaft. The lower end is rotated later-ally in relation to the upper, thus

Figure 4. A. Successive femoral diaphyses of infants ranging from newborn to adult fromright to left. The angular remodeling of the femur induced by the transition is shown froman abducted knee to an adducted knee. The immature diaphyses are devoid of theirepiphyses. B. Radiograph of the lower limbs of a 7-year old boy who had never walked.The femoral diaphysis is vertical in relation to the physeal plane. [Color figure can beviewed in the online issue, which is available at wileyonlinelibrary.com.]

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exhibiting ‘‘lateral’’ torsion, which ismeasured between the transverseintercondylar axis of the upper endand the transverse intermalleolar axisof the lower, as projected in a hori-zontal plane34–36 (Fig. 3). I observeda lateral torsion of 58 in an intactnewborn tibia. Tibial torsionincreases during postnatal growth.The measurement of this angle is dif-ficult to compare between adults andchildren. In adults, measurementsare collected directly on dry bones,while in children clinicians use indi-rect in-vivo techniques. No in-vivotechnique measures true tibial tor-sion.37 On 50 adult dry tibias, themean angle of tibial torsion was 298(extreme values: 08–428).38 By CTscan measurements, Kristiansenet al. found a mean of 388 in 26adults (extreme values: 188–478) anda mean of 288 in 14 children between3–5 years (extreme values: 208–378).

Femoral Antetorsion Is Typicallyin the Opposite Direction FromTibial Torsion

Rotation in one element mighttherefore be compensated for by acounter-rotation in the other ele-ment.38,40,41 In a sample of 50 adultcadavers, Kobylanski38 noted a weakcorrelation of 0.44 (P > 0.01). Infact, femoral antetorsion and tibialtorsion are never tightly correlated inlarge samples.36,42

Most often, the angle of anteversionof the neck, which is high at birth,decreases by 2 or 3 years of age. Some-times it remains high until 7 years ofage or later. This high angle, when thefemoral head is properly seated in theacetabulum, places the distal femur inmedial rotation so that the two patellaeare medially oriented. The feet then toein. If usually tibial torsion achieves itsadult level around the sixth year ofchildhood,32 in these cases tibial torsionoften increases after 7 years (Fig. 8). Thelarge femoral anteversions limit the lat-eral rotation of the hip and close theangle of gait, while the tibial torsionopens the angle of gait.29

During the single-support phasesof gait, the body weight tends to tiltthe trunk medially about the acetab-ulum. This is resisted by the tensionof the abductor muscles (glutei mini-

mus and medius and tensor of fascialata). Rotation of the femur inter-nally or externally from its neutral

Figure 8. A. 6-year-old girl presenting a high anteversion angle (408) of the femoral neck,placing her knees in medial rotation so that the patellae (red circles) are facing eachother. Consequently, the feet are toeing in. B. In this adult, the anteversion of the neckwas maintained at a quite high degree, but because of the lateral rotation of the tibiathe feet are parallel (after Kendall42). C. In this normal adult, the anteversion of the neckis decreased and the tibial torsion is increased slightly (after Kendall42). D. In this boy, theanteversion of the neck is decreased and the patellae are located centrally, but thelateral torsion of the tibia is very high (408), so that the feet are placed apart. [Color fig-ure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 6. A. Proximal femur of a) a new-born and b) an infant between 3 and 6months of age. B. Development of theHarris lines, which appear on the femoralneck after an arrest of growth. C. Subadultproximal femur with the capital epiphysisand the greater trochanterian apophysisunfused. The apophyseal angle (AA)remains constant during growth. The epiphy-seal angle (EA) increases during growth.

Figure 7. A. Increase in utero anddecrease in postnatal life of the antever-sion angle of the femoral neck. B. Whenthe pressure is strong in the maternal uterus,the fetus adopts a position that necessitateshyperflexion of the lower limbs. A first-orderlever system is thus created: The force (F) isgenerated at the level of the neck by fem-oral flexion. The resistance (R) comes fromthe acetabulum. The support point islocated between the femur and the pelvisacross the soft tissues (a). The force F wouldbe responsible for the progressive torsion ofthe femoral diaphysis through the dynamicsof bone tissue remodeling (modified fromLe Damany34). [Color figure can be viewedin the online issue, which is available atwileyonlinelibrary.com.]

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position necessitates increased ab-ductor muscle forces to maintain alevel pelvis: 308 of internal or exter-nal rotation would entail supplemen-tary work for the gluteus medius of30 pounds by changing the orienta-tion of its fibers (Fig. 9).43

FEMORO-PATELLAR JOINT

Femoral Trochlea

Femoral obliquity has an impor-tant direct consequence on the orien-tation of muscular forces at the kneeand consequently on the shape of thedistal femoral epiphysis. In bipedalhumans with a valgus orientation ofthe femur, the patella, inserted in thedistal tendon of the quadriceps mus-cle, is subjected to a lateral force vec-tor due to femoral obliquity. In thehuman knee, the femoral trochlea isdeepened by a central sulcus and itslateral lip is prominent. The protu-berant lateral lip of the femoraltrochlea guards against any lateraldislocation of the patella during

extension of the knee joint. Figure 10shows the movement of the patellaas viewed from above with the troch-lear groove in full extension and indifferent degrees of flexion. In greatapes, which exhibit a habitual flexedposition of the knee joint and lackthe valgus angle, the trochlea is flat andits medial and lateral sides are symmet-rical. The patella is free to move, partic-ularly during the frequent rotationalmovements of the knee (Fig. 11).

The variability of the human troch-lear shape is high. There is no rela-tionship between the degree of femo-ral obliquity and the degree of prom-inence of the lateral lip either duringgrowth or in the adult.45,46 Surpris-ingly, the protuberance of the laterallip of the femoral trochlea and thetrochlear groove are already presentin the fetus and newborn.14,16,47

Evolution of trochlear shape?

The angle of femoral obliquityappears in the human infant before 2

years of age. This angle appeared inthe first hominids at an even earlier age,since their growth was shorter.56,57 Thetrochlear sulcus and the prominence ofthe lateral lip are present in the fetusand newborn with the same variabilityas in adults. Two hypotheses can be pro-posed. Either the deepened trochlea witha salient lateral lip was randomlyselected, which is unlikely, or it wasselected following the process of geneticassimilation.58,59 The hominid femoro-patellar joint would have been reshapedin two steps involving a partly epigeneticand partly genetic process.14,16,54

In late australopithecines or earlyHomo, the prominence of the laterallip of the femoral trochlea would havebeen formed as a response to the lat-eral stimulus of the patella duringpostnatal life. Two arguments supportthis. First, in cases of congenital dislo-cation of the patella, the trochlea isflat. After surgery to realign andrecenter the patella in young children,the trochlea deepens after some yearsby epigenetic action. However, the de-velopment of the groove in such chil-dren could also be interpreted as adelayed expression of a genetic traitnormally expressed in utero.In the course of the evolution of

Homo, this lateral stimulus wouldhave been superseded by an internalgenetic factor. The use of full kneeextension was clearly selected for inlater hominin evolution.14,15 A veryweak protuberance of the lateral lip ofthe femoral trochlea (a hollow sulcus)is present in the fossil AL 129 1a, butthere is no sustrochlear hollow(depression at the top of the patellargroove). However, in Homo habilis thesulcus is deep, the lateral lip is highand a ‘‘sustrochlear hollow’’ is present,illustrating the capacity of full kneeextension, which is absent in A. afaren-sis (Fig. 11D). In modern humans, thepatella sits in the sustrochlear hollowwhen the knee is completely extended.

FEMORO-TIBIAL JOINT

Shape and Tibial Insertions ofthe Interarticular Menisci

In hominid evolution, the knee-joint evolved from having a singleinsertion of the lateral meniscus onthe tibia to a double one.60–62 WhileAustralopithecus afarensis exhibits a

Box. 2. Patellar Luxation

Patellar luxations are almostalways lateral. Very often, luxationoccurs when the patella moves fromits highest position in the sus-troch-lear hollow (Fig. 10B red arrow) thetrochlear groove.48 Luxations occurmostly on flat trochlea.48–52 Weshowed that such dysplatic flat troch-lea are already present in some fetusesand newborns (Fig. 12).53,54 Flattrochlea can be interpreted either as areversion, which we believe, or as a

convergencewith the trochlea of greatapes. Flat trochlea are found in Mio-cene primates such asPaidopithex rhe-nanus and Pliopithecus vindobonen-sis.49 The trochlea of Australopithecusafarensis appears to be far flatter thanthat of Homo habilis (Fig. 11D).Recurrent luxations withmajor troch-lear dysplasies were found in differentmembers of a single family,55 suggest-ing that genetic factors are likelyinvolved in this pathology.

Figure 12. A. Radiographs of a normal femoro-patellar joint and a subluxated one. Luxa-tion is always lateral. B. Patellar luxation. C. Upper row: Adult dysplasic flat trochlea on afemur and on radiographs. Lower row: Flat trochlea can be observed in one newbornand three fetuses. [Color figure can be viewed in the online issue, which is available atwileyonlinelibrary.com.]

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single insertion, early Homo clearly hasa double insertion of the lateral menis-cus on the tibia (Fig. 13). This supple-mentary insertion restricts the mobilityof the meniscus on the tibial plateauand prevents a too-large anterior dis-placement of the meniscus in fullextension. It indicates a habitual prac-tice of full extension movements of theknee joint in the stance and swingphases of bipedal walking. This addi-tional posterior insertion of the lateralmeniscus appears early in human fetallife.63,64 Consequently, in early Homo,this feature likely developed as theresult of a genomic change.The occurrence of a single anterior

insertion of the lateral meniscus inextant humans appears occasionallyas a pathology.65,66 It is the cause ofpain and dysfunction of the kneejoint,and can be interpreted as a reversion.Although this analysis is restricted

to lower limb features, it reveals that

a principally epigenetic feature, thefemoral bicondylar angle, following a

genetic modification of the pelvis,would have acted as the initial switchthat set in motion selection for a cas-cade of features under the influenceof increased use of full extension ofthe knee joint. This cascade of inter-related features improved the effi-ciency of bipedal walking, as habitualuse of full extension of the knee is anessential component of the modernhuman striding gait.Depending on the nature of the

structures involved, either diaphysisor epiphysis involving the replace-ment of cartilage by bone tissue or ameniscal insertion involving the dif-ferentiation of a ligament, weobserve that evolution involved bothgenetic and epigenetic changes. Theaxial growth of the diaphysis, bymeans of a discoid growth cartilageat its distal end, implied an epige-netic angular remodeling; the differ-entiation of the meniscal ligamentimplied a genetic change. The epiphy-ses are developed from a sphericalgrowth cartilage that grows centripe-tally. The multidirectional growth ofthe epiphysis would have implied atwo-stage modification: an initial epige-netic change during postnatal life andthen a genetic assimilation of this change.

THE FOOT AND LOSS OF ITSPREHENSILE ORIGIN

The human foot today is exclu-sively terrestrial, adapted to bipedal

Figure 10. A. Sagittal radiographs of the kneejoint in full extension: The patella is locatedin its highest position, above the trochlea, in the sustrochlear hollow. B. Inferior view ofthe knee joint: successive positions of the patella from full extension to 1208 of flexion. Thepatella is located in the sustrochlear hollow (black arrows). The red arrow shows the mostfrequent path of patellar luxation. [Color figure can be viewed in the online issue, whichis available at wileyonlinelibrary.com.]

Figure 9. Horizontal views of the pelvis with the right femur placed in progressive degreesof medial rotation (A) and in 308 of lateral rotation (B). The angle of anteversion of thefemoral neck is normal, around 158. The green lines show the direction of the femoralneck, the red lines the direction of the knee and patella (after Merchant43). C. Coronalview of the pelvis tilted anteriorly 208: Direction of the mean fibers of the gluteus mediusin the position of high lateral rotation of the femur. This oblique direction could be one ofthe causes for the supplementary work generated by this muscle in this position. Thesame reasoning can be used when the rotation is medial and extreme, resulting in anopposite oblique direction (after Kapandji44). [Color figure can be viewed in the onlineissue, which is available at wileyonlinelibrary.com.]

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support and propulsion. However,our foot was originally a graspingand prehensile organ. Two hallmarksof the bipedal foot are the adductionof the first toe toward the other toesand the presence of a plantar arch(Fig. 14).The great toe branches from the

sole of the foot, just at the base ofthe second toe in the early growthstages of all nonhuman primates. Inthe early embryogenesis of thehuman foot, a major shift occurred.This embryonic position is retainedthroughout life in humans,69

whereas in other primates the placeof attachment of the great toe shiftsproximally (Fig. 14 A, B), similar tothe ontogenetic shift in the attach-ment of the thumb to the palm fromthe base of the index finger to aplace nearer to the wrist. Conse-quently, the web that binds the firstand second toes persists in thehuman foot and no cleft is formed.Thus, no abduction and no rotationof the hallux are permitted. Thisembryonic change was one of the

major transformations, perhaps thefirst, from a grasping foot to a ter-restrial foot adapted to support andpropulsion.

Was this transformation drastic,

happening in a single step, as sug-

gested by the embryogenesis, or was

this transition progressive and grad-

ual, as some authors,70–72 based on

the provisional interpretation of a

fossil hominid foot (cuneiform Stw

573), propose? ‘‘These intermediate

stages may appear as modifications

of the medial cuneiform first meta-

tarsal joint where it becomes less

medially oriented and flatter through

time.’’71 In fact, the gradualism is

not confirmed by existing hominid

fossils: ‘‘Hallucial convergence was

substantially complete in both Aus-

tralopithecus afarensis and africanusand in Homo habilis. The feet of

these hominids can therefore be con-

sidered to have remodelled so as to

have lost the ability to oppose the

hallux and therefore operate a grasp-

ing foot.’’71 However, Lewis73 and

other authors74 interpreted the fossil

foot OH 8 (Homo habilis) as apelike

with arboreal adaptations including

an abductable hallux. Conversely,

other authors,70,71,75 among them

Susman,76 strongly suggested ‘‘reso-

lute adaptation to human bipedal-

ism’’ based on ‘‘the total morphologi-

cal pattern including the foot and

the associated leg of OH 35.’’The second feature characteristic

of the human bipedal foot is thepresence of a plantar arch (Fig. 14E). In the newborn, the plantar archis present before walking, but isobscured by the thickening of theplantar cushion. The early adductionof the great toe and the early pres-ence of the plantar arch are some-times used as arguments to refute theprehensile origin of the human foot.77

This is contrary to all available evi-dence from comparative anatomy.

Figure 13. A. Superior view of right tibiaswith the medial and lateral menisci andtheir tibial insertions in great apes andhumans. The posterior insertion of the lateralmeniscus, exclusive of humans, creates anotch on the posterior border of the tibialplateau. B. This notch is absent in Australo-pithecus afarensis (AL 129) and present inHomo habilis (ER 1481). [Color figure can beviewed in the online issue, which is avail-able at wileyonlinelibrary.com.]

Figure 11. Chimpanzee (A) and human (B)femora and their distal epiphysis and pa-tella in inferior view. C. The human angle offemoral obliquity implies an oblique directionof the quadriceps muscle, inserted on theproximal tibia so that a lateral force isapplied to the patella. D. Inferior views ofthe distal femoral epiphyses of different hom-inid fossils showing the very low lateral lip inAustralopithecus afarensis and the deeptrochlear groove in Homo habilis. [Color fig-ure can be viewed in the online issue, whichis available at wileyonlinelibrary.com.]

Figure 14. Embryogenesis and adult stateof the right foot of some primates. A. Threestages of the embryogenesis of the foot ofa macaca at 44, 66, and 75 days of age,showing the proximal migration of the firsttoe. Adult state on the right (afterSchultz67). B. Early stage of the embryo-genesis of the human foot of 44 days, ascompared with the adult state, showingthe retention of the distal position of thefirst toe (after Schultz67). C and D. Adultfoot of a chimpanzee and a human, plan-tar view (C), dorsal view (D) (afterSchultz68). E. Lateral view of radiographs ofa human foot with its plantar arch. (A-D :Not to scale. All the feet are standardizedto the same length.)

ARTICLES 181

Arguments for a PrehensileOrigin of the Human Foot

In the first arguement, Keith78

noted that in the ape’s foot the ten-don of the flexor hallucis longuspasses through a ligamentous loop atthe base of the first metatarsal bone(Fig. 15), a structure that maintainsthe tendon in its proper positionwhether the foot is abducted oradducted. A remnant of this looppersists in the human foot, telling usof a time when the great toe of manenjoyed a mobility that has longbeen denied to it.Keith78 argued that the hallux did

not adduct toward the other toes butthat the other toes adducted towardthe great toe. To support this hy-pothesis, he compared the feet of ahuman newborn and a gorilla (Fig.16), noting that the relationships ofthe first metatarsal to the tarsus arealike in both. What has changed isthe axes of the second, third, andfourth toes, which have swunginward toward the great toe. For along time, I thought this comparisonwas a strong argument. However, thenewborn human foot used in thiscomparison was a pathologic foot. Itwas a skewed foot with a seriousmetatarsus varus (Seringe, personalcommunication). At the time ofKeith’s study, these pathologies hadnot yet been diagnosed. Conse-

quently, this comparison fails to sup-port the argument.

Lewis79 followed Keith,78 propos-ing the model of the loss of foot pre-hensility. Lewis’ functional consider-ations are very strong, mostly basedon the importance of the direction ofthe subtalar axis, which makes amore acute angle with the long axisof the foot in humans than in theapes. He argued that it is around theaxis of the subtalar joint that theentire foot would have been real-igned. Aiello and Dean80 gave a perti-nent summary of this hypothesisand its morphological implications:‘‘Lewis suggested that the adductedhuman great toe has been brought inline with the remaining toes as theresult of the realignment of the lat-eral four metatarsal towards the firstmetatarsal and the oblique subtalaraxis rather than the realignment ofthe first metatarsal towards the fourothers and away from the subtalaraxis.’’ Is this interesting propositioncompatible with the embryogenetictransformation mentioned earlier? Isit compatible with a rapid change?The questions remain open.

Lewis79 proposed another line ofevidence by examining the morphol-ogy of the first cuneo-metatarsaljoint. In the grasping foot, the tibialisanterior presents two distal heads;the first inserts on the cuneiform, thesecond on the metatarsal (Fig. 17).The articular surface of the cunei-form presents an upper convexityconfluent below and medially withan oblique groove that ventrallyforms a concavity. The upper por-tion, spiralling onto the medial as-pect of the bone, represents theimpression of the metatarsal tendonof the tibialis anterior. Abduction ofthe first ray is accompanied by arotation, locking the margin of themetatarsal into the inferior concavityof the cuneiform. The joint is then ina close-packed position. In humans,the dual insertion of the tibialis ante-rior is retained; even if the anteriorarticular surface of the cuneiform iscommonly flat, it is variable andsometimes shows a morphology rem-iniscent of that of the great apes(Lewis, Aiello and my own observa-tions). The cuneiform of the fossil

AL 333 (Australopithecus afarensis) isinterpreted in this context.81

TOWARD AN INTEGRATIVEANALYSIS

In the first part of this review, weillustrated the principal angularchanges in the femur and tibia thatcontribute to formation of the direc-tional axes of the lower limbs.According to Saraffian,82 anotherchange should occur during growthat the tibiotarsal joint. In the new-born, this joint should not be hori-zontal (Fig. 18); the correction of itsvalgus position should occur onlyaround twelve years of age. This im-portant frontal change needed verifi-cation because it introduces a strongimbalance between the interarticularline and the growth physeal line ofthe kneejoint. A recent study basedon a large sample of childrens’ radio-graphs invalidated this observation.The tibiotarsal joint and the epiphy-seal line are horizontal at the neona-tal state and further on.83

An important step in integration isunderstanding of functional relation-ships, not between the tibia and the

Figure 16. Comparison made by Keith78

between the foot a human newborn anda gorilla in dorsal view showing the inwardbend of the outer four metatarsal bones inthe first one in relation to the gorilla. Weinvalidated this comparison since the new-born foot is a pathologic one, undiag-nosed at the time of Keith. [Color figurecan be viewed in the online issue, which isavailable at wileyonlinelibrary.com.]

Figure 15. A. Muscles of the great toe inthe prehensile foot of a pronograde mac-aque: adductor muscles (green), flexorhallucis longus (red), and its ligamentousloop at the base of the first ray. B. Thesame muscles in the foot of a human new-born with the atavistic loop at the base ofthe hallux (after Keith78). [Color figure canbe viewed in the online issue, which isavailable at wileyonlinelibrary.com.]

182 ARTICLES

foot, but between the talo-tibio-fibu-

lar unit and the remaining foot, thecalcaneo-pedal block, also called

lamina pedis (Fig. 19A).84,85 During

walking, the medial or lateral axialrotations of the lower limbs are con-

stant; the adaptation of the foot tothe ground is effected through this

articular complex, permitting the

calcaneo-pedal block to transform

the underlying axial rotation alongits longitudinal axis. The movements

between these two units occur

around the subtalar axis or talo-cal-caneo-navicular axis, which is ori-

ented obliquely downward, back-ward, and outward (Fig. 19B).84,85

The talofibular unit is articulated

with the calcaneo-pedal block bythree joints (posterior and anterior

subtalar joints and talo-navicularjoint). Under weight-bearing condi-

tions, displacements occur in thiscomplex joint as compensation for

the rotational displacements occur-ring in the upper part of the limb

(Fig. 19C).The postcranial skeleton is an inte-

grated system, particularly in thebipedal human. The different ele-ments of this articular chain, includ-ing the vertebral column, pelvis, andlower limbs, function in vivo inclosely coordinated fashion to copewith constraints imposed by gravity.The challenge is to ensure an efficientbalance during standing and walking.It is important to find the rela-

tionships that link the lower limbs,studied here, and the pelvis. Theformation of the directional axes ofthe lower limbs during growth thatwe have described depends, on onehand, on the reaction forces comingfrom the ground during gait acquisi-tion but, on the other hand, on thedownward forces coming from thepelvis through the acetabula, withthe three-dimensional orientation ofthe acetabula being the critical pa-rameter. The variability of this pa-rameter in humans86–89 probablyplays a role in determination of theaxes of the lower limbs we havedescribed here. I called this acetabu-lar parameter, including its degreeof anteversion, inclination, and sphe-ricity of the acetabula, the ‘‘functionallink’’ between the pelvis and lowerlimbs.86 While the anteversion of thefemoral neck decreases during growth,we showed that the anteversion of theacetabula decreases. For mechanicalreasons, their relationships are antago-nist during learning to walk.89

Upward, the functional linkbetween the pelvis and vertebral col-umn is assessed by a sagittal pelvicparameter, the sacral incidenceangle, discovered clinically on radio-graphs of the pelvi-rachidian unit90,91

and morphologically described fromsamples of ostelological pelves.86–89

CONCLUSIONS

Developmental studies show thecomplex implication of genetic and

Figure 18. Tibio-talar joint in a newborn, a 12-year old child, and an adult passing froma valgus position to a horizontal position. Lateral side indicated by the fibula. A recentstudy showed that this observation is wrong: the epiphyseal line and the tibiotarsal jointare horizontal as soon as the neonatal state (after Sarafian82).

Figure 17. A. Tibialis anterior in humans. B. First cuneo-metatarsal joint in a gorilla foot.Red area (1) on the cuneiform: insertion of the first tendon of tibialis anterior (c. T. ant.),red area (2) on the metatarsal bone: insertion of its second tendon (m. T. ant.). Whenthe grasping pincer is closed, this tendon passes on the concave articular surface of thecuneiform (elongated red area). C. Inferior view of the cuneiforms of Gorilla. The first onecorresponds to the shape of the one in B (from Lewis73). [Color figure can be viewed inthe online issue, which is available at wileyonlinelibrary.com.]

ARTICLES 183

epigenetic factors. In this review, wehave described first the epigeneticfeatures that result from habitualbehavior during development. Theyinclude all the angles that eitheropen or close: the angle of obliquityof the femur, the neck-shaft angle,and the angles of femoral and tibialtorsion. The formation of these

angles, which is linked to the com-bined effects of gravity, muscular ac-tivity, and growth, is well explained,given the malleability of the largelycartilaginous skeleton of the infant.The action of gravity in loading theskeleton and during gait acquisitionis very important, as indicated by theabnormal morphology of nonwalking

children. The way in which the skele-ton is loaded, as well as the waywalking is learned, is specific to eachindividual. The variability of thedescribed angular parameters illus-trates this singularity. The integra-tion among all these parameters isalways the result of the intrinsicfunctional behaviors of an individual.

Figure 19. A. Talo-tibio-fibular unit (white) and calcaneo-pedal block (yellow). The talus is fixed in the bimalleolar mortise. B. Subtalar axis.C. Subtalar axis transmits the medial rotation of the leg to the foot along its longitudinal axis. The lateral fore foot is carried in pronation.To remain plantigrade, a supination twist is applied to the medial forefoot (after Seringe and Wicart84). [Color figure can be viewed inthe online issue, which is available at wileyonlinelibrary.com.]

184 ARTICLES

The skeleton is also subjected tofunctional constraints during prena-tal growth. The example of the angleof femoral anteversion, which opensduring prenatal growth and closesduring postnatal growth, is emblem-atic, and can illustrate the oppositenature of the constraints that act onthe skeleton both in utero and post-natally.It can almost be considered a tru-

ism that the locomotor skeleton isfirst and foremost genetically deter-mined. The retention of the distalposition of the hallux at the base ofthe second toe is emblematic of thiscategory. The presence of a posteriorinsertion of the lateral meniscus onthe lateral tibial plateau in earlyhuman embryogenesis is also clearlya genetic feature resulting fromselection.Among the epigenetic characters,

we think that the angle of femoralobliquity deserves special status,since its presence in hominid fossils,following a genetic modification ofthe pelvis, would have been an ‘‘ini-tiator’’ feature. It set in motion selec-tion for a series of features of theknee joint, such as meniscal inser-tion, trochlear shape, and the sus-trochlear hollow, under the influenceof an increasing use of full extensionof the kneejoint. Depending on thenature of the structures involved—diaphyses, which grow axially, epi-physes, the growth of which is multi-directional and involves the replace-ment of cartilage by bone tissue, ormeniscal insertion, which involvesthe differentiation of a ligament—weobserved that evolution proceeded byinteracting epigenetic, geneticallyassimilated, and genetic changes.The pathology described in this

review, patellar luxation, illustrates aninteresting aspect of human evolution.Each adaptation represents a compro-mise: Decisive advantages would beassociated with risks or possible disad-vantages. The risk of patellar luxationis a slight disadvantage as comparedto the economy provided by anadducted knee during walking.We observed that study of the

growth of the lower limb is typicallydone either in the frontal plane or inthe horizontal plane, depending onthe features studied. True three-

dimensional investigations are stillrare. In the next decades, it will beimportant to fill this gap. Finally,since the whole locomotor skeletonis an integrated system, it is, ofcourse, artificial to separate lowerlimbs from the pelvis and vertebralcolumn. A systemic analysis of thewhole articular chain during growthwould be a promising challenge tounderstand the coordination of allthe pieces of this complex, integratedsystem.

ACKNOWLEDGMENTS

I thank R. Seringe and P. Wicart,orthopedists in the hospital SaintVincent de Paul in Paris, for thenumerous questions they answeredabout the growth processes in chil-dren, while trying to identify the nor-mal growth processes through thedifferent abnormal ones. I am grate-ful to Y. Glard, orthopedist in thehospital of Marseille, for his helpconcerning the correlations betweentibial torsion and femoral antever-sion, and to J.P. Damsin, orthopedistin the hospital of Armand Trousseauin Paris, for all the clinical growthdocuments he provided to assess myresults. Financial support was pro-vided by the A.T.M. (Action Thema-tique du Museum) ‘‘Formes possi-bles, formes realisees.’’ I am indebtedto A. Herrel for fruitful discussionsand for his help in the English trans-lation, and to my two students, N.Bonneau and L. Canard, for the con-tribution of their own research.

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