2012-Richmond & Jungers

248

Abstract

The proximal femur has played a prominent role in our understanding of

the origin and evolution of human gait because of its functional importance

and relatively good representation in the fossil record. This study examines

the morphology of femora from the fossil record, including those attrib-

uted to Orrorin tugenensis (BAR 1002’00) and Homo fl oresiensis (LB1/9).

Considerable debate surrounds both of these taxa, focusing primarily on the

evidence that the former is a hominin and shows convincing adaptations for

bipedalism , and over whether or not the latter is a pathological diminutive

modern human or a distinct species (and what the anatomy suggests regarding

the evolutionary history of H. fl oresiensis ). This study addresses the questions

of whether Orrorin femoral morphology more closely resembles femora of

humans and fossil hominins than apes, and whether it is more similar to the

femora of Homo among the hominins. Our study also tests the hypothesis that

the femoral morphology of LB1/9 is consistent with that of a small-bodied

modern human, or more closely resembles fossil hominins. To test these ques-

tions, we compare the proximal femoral morphology of BAR 1002’00 and

LB1/9 to a large sample of adult humans, chimpanzees, bonobos, gorillas,

orang-utans and most available early hominin taxa. Importantly, the human

sample includes individuals from large- and small-bodied populations that

overlap with the small sizes of BAR 1002’00 and LB1/9.

The results show that the external morphology of the Orrorin femur more

closely resembles the femora of Australopithecus and Paranthropus than those

of great apes, or fossil and modern Homo . Its morphology is not consistent

with it being characterised as more like human than australopith femora, or

a phylogenetic hypothesis that Orrorin is ancestral to Homo to the exclusion

of the australopithecines. However, its morphology is consistent with its 6

13 Hominin proximal femur morphology from the Tugen Hills to Flores

Brian G. R ichmond and

William L. Jungers

African Genesis: Perspectives on Hominin Evolution , eds. Sally C. Reynolds and Andrew

Gallagher. Published by Cambridge University Press. © Cambridge University Press 2012.

Hominin proximal femur morphology 249

million-year-old age and its taxonomic assignment as a basal, bipedal hominin.

The external morphology of the Orrorin femora shares similarities with those

of gracile and robust australopiths despite some evidence suggesting more

primitive cortical structure, raising potential questions about hip function in

Orrorin . The proximal femoral anatomy of LB1/9 shows that it is not a small

modern human, and instead supports evidence from other anatomical regions

that it represents a distinct species, Homo fl oresiensis , with strikingly primitive

femoral morphology resembling early hominins.

Introduction

In studies of the origin and evolution of human gait, the proximal femur has

played a prominent role because of its functional importance and relatively

good preservation in the hominin fossil record. While there is broad agree-

ment that femoral anatomy varies over the course of human evolutionary his-

tory, some disagreements continue over what morphology characterises certain

taxa, and major debates persist over the mechanical and behavioural implica-

tions of this morphological variation.

Numerous researchers have studied the femoral anatomy of gracile and

robust australopiths (e.g. Napier, 1964 ; Day, 1969 , 1973 ; Robinson, 1972 ;

Lovejoy et al. , 1973 ; Walker, 1973 ; McHenry, 1975 ; Wood, 1976 ; McHenry

and Corruccini, 1976a , 1978 ; Stern and Susman, 1983 ; Lovejoy, 1988 ; Jungers,

1991 ; Ruff, 1995 , 1998 ; Lovejoy et al. , 2002 ; Richmond and Jungers, 2008 ;

Harmon, 2007 , 2009a , b ). Perhaps the most important functional characteristic

is femoral length, which in Australopithecus afarensis is intermediate between

African apes and humans (Jungers, 1982 ). Compared with modern humans,

the proximal femur of Australopithecus and Paranthropus is characterised by

a long and anteroposteriorly-narrow neck, small head, superiorly projecting

and laterally fl at greater trochanter, and a robust femoral shaft (see references

above). Some have debated whether Australopithecus had a relatively small

femoral head (e.g. McHenry and Corruccini, 1976a , b ; Jungers, 1988 , 1991 )

or not (e.g. Wolpoff, 1976 ; Ruff, 1998 ). Researchers mainly disagree over the

choice of the most appropriate size variable against which to compare the size

of the femoral head (see below).

The femoral anatomy of early Homo is unique, differing from that of austral-

opiths and modern humans. Relative femur length is similar to modern humans

in early H. erectus (Ruff and Walker, 1993 ; Lordkipanidze et al. , 2007 ) and dif-

fers signifi cantly from that of A. afarensis (Richmond et al. , 2002 ). However,

proximal femur shape is unique in early Homo , with a large femoral head, long

femoral neck (primitive) and wide mediolateral (ML) shaft, with its narrowest

Brian G. Richmond and William L. Jungers250

point occurring more distally than in modern humans. Ruff ( 1995 ) makes a

convincing argument that the great mediolateral shaft width and low position

of minimum breadth are biomechanically related to elevated bending moments

that would result from the long femoral neck, and potentially laterally fl aring

ilia, retained in early Homo .

It was relatively late in human evolution that we fi nd evidence of a short

femoral neck and reduction in the breadth of the femoral shaft (Ruff, 1995 ). By

the Middle Pleistocene, femora (e.g. Gesher Benot Ya’acov 1, Israel ) no longer

have the ML-broad and relatively AP-narrow proximal shaft shape seen in H. erectus . Thus, archaic Homo has a more human-like proximal femur shape

with large femoral heads, short femoral necks and more rounded proximal

shafts (Ruff, 1995 ).

As noted above, where researchers have debated over how to characterise

fossil hominin proximal femur morphology, the main source of discrepancy

has been the choice of size variable used to standardise the sizes of other vari-

ables (e.g. McHenry and Corruccini, 1976b ; Wolpoff, 1976 ; Jungers, 1988 ,

1991 ; Ruff, 1998 ). Femoral head size has functional implications because large

joint sizes are related to high joint loads and/or high levels of joint mobility

(Godfrey et al. , 1995 ; Ruff, 2002 ). Some who argue that Australopithecus had

a modern human-like relative joint size interpret the gait of Australopithecus as

being essentially modern human-like. Some who argue that femoral head size

is small in Australopithecus interpret the small joint size as indicating relatively

low levels of loading; this in turn suggests that while bipedal, Australopithecus

was not adapted for running or walking long distances (e.g. Stern and Susman,

1983 ; Jungers, 1988 ; Bramble and Lieberman, 2004 ). Others point out that

the small femoral head is part of a biomechanical complex including a long

femoral neck and therefore more effective moment arm for the gluteal muscle

action during gait (Lovejoy et al. , 1973 ; Ruff, 1998 ), leading some to interpret

Australopithecus as having the ‘expected’ head size (Lovejoy et al. , 1973 ) or

a head size still smaller than expected within its biomechanical environment

(Jungers, 1991 ; Ruff, 1998 ). These differences of opinion can be traced in part

back to phrasing the question in different terms of ‘relative size’, shape per se

versus mass-adjusted size of the femoral head.

In this study, we use the geometric mean of proximal femur measurements

because the geometric mean is a size surrogate that has proven to reliably pre-

serve shape information in scaling studies (Jungers et al. , 1995 ), and allows

us to assess whether anatomical features such as the femoral head are small

relative to the rest of the proximal femur. Restricting our variables to those

preserved on the proximal femur also allows us to include a relatively large

sample of fossils (e.g. compared to methods requiring other associated elem-

ents or known/estimated body mass; Auerbach and Ruff, 2004 ).


We evaluate the pattern of shape variation in a sample of Miocene-Pleistocene

hominin femora against a large sample of extant great apes and samples of six

modern human populations spanning the human size range. To this sample, we

add the proximal femora belonging to two recently described taxa from the

very earliest and latest periods of the hominin fossil record, Orrorin tugenensis

( c . 6 Ma) and H. fl oresiensis (Late Pleistocene), in order to examine how they

compare with the femora of other hominins.

Since its initial discovery, researchers have debated whether or not the

femoral morphology of Orrorin indicates that it was adapted to bipedality.

Although numerous qualitative traits (e.g. obturator externus groove, relative

femoral head size, relatively long neck) are consistent with bipedalism, each

of them occur to some extent in other primates and therefore do not conclu-

sively indicate that Orrorin was bipedal. For example, the obturator externus

groove is often cited as a bipedal trait, but it is not unique to humans. As vari-

ous authors have noted, the obturator externus groove occurs in other primates

such as Ateles and Papio as well as humans. Its presence therefore indicates

‘frequent bipedalism’, including bipedalism practised by monkeys and apes

(Stern and Larson 1990 ; Stern and Susman 1991 ; Pickford et al. , 2002 ). Other

features of the Orrorin femoral anatomy would benefi t from an analysis using

quantitative statistical methods. For example, Senut et al. ( 2001 ) and Pickford

et al. ( 2002 ) note that the femoral head in Orrorin is larger relative to its shaft

than it is in A.L. 288–1 (the A. afarensis specimen from Hadar commonly

known as ‘Lucy’). However, in this measure, A.L. 288–1 has a femoral head

size comparable to those of great apes, and it is unclear whether or not the

Orrorin femoral head (BAR 1002’00) is signifi cantly larger than those of apes.

Similarly , Orrorin is described as having a long femoral neck (Senut et al. , 2001 ; Pickford et al. , 2002 ; Galik et al. , 2004 ), but quantitative analyses are

needed (Richmond and Jungers, 2008 ).

Analyses of CT images of BAR 1002’00 have led to confl icting interpret-

ations. An initial study (Galik et al. , 2004 ) of femoral neck cortical distribu-

tion concluded that the ratio of the inferior to superior cortical bone thickness

in BAR 1002’00 is high as in modern human femora. More recent analyses

of those CT scans concluded that the skewness of femoral neck cortical dis-

tribution more closely resembled chimpanzee than modern human femora

(Kuperavage et al. , 2010 ), although the data showed considerable overlap

among the samples. Others have argued that the CT scans are unfortunately too

coarse to reliably characterise the internal morphology (Ohman et al. , 2005 ).

At present, the cortical geometry evidence has not resolved debates about

bipedalism in Orrorin .

Senut et al. ( 2001 ) also argue that BAR 1002’00 is morphologically more

human-like than Australopithecus femora, and propose that Orrorin is ancestral


to Homo while Ardipithecus and Australopithecus are not. These authors

subscribe to the relatively uncommon view that the Hadar hominins represent

two taxa – Australopithecus afarensis and Praeanthropus afarensis , in which

they argue the former comprises a clade with other Australopithecus species

and with Paranthropus , and the latter they argue to be ancestral to Homo .

This study builds on recent work (Richmond and Jungers, 2008 ) to address

the questions about how Orrorin femoral morphology compares with femora

of humans, fossil hominins and apes, and whether the morphology is more

similar to the femora of Homo compared to those of other early hominin taxa.

At the other end of the temporal spectrum, the recent discovery of skel-

etal elements attributed to H. fl oresiensis on the Indonesian island of Flores

(Brown et al. , 2004 ; Morwood et al. , 2005 ) has raised many questions about

the nature of these remains, especially whether the remains represent patho-

logical modern humans, or a dwarfed taxon with a long evolutionary his-

tory. Much of the debate has focused on brain and skull size and shape, with

some arguing that LB1/9 displays the morphology consistent with micro-

cephally and/or other pathologies in modern humans (Weber et al. , 2005 ;

Jacob et al. , 2006 ; Martin et al. , 2006a , b ; Richards, 2006 ; Hershkovitz et al. , 2007 ) and others refuting this conclusion and demonstrating similarities in

cranial and endocranial shape with early hominins, including early Homo

and even Australopithecus (Falk et al. , 2005 , 2007 , 2009 ; Argue et al. , 2006 ;

Gordon et al. , 2008 ). Evidence from the postcranium suggests that the Liang

Bua skeletal remains come from a hominin with primitive morphology,

notably limb proportions including a relatively short femur and long fore-

arm (Morwood et al. , 2005 ), robust limb bones (Jungers et al. , 2009a ), a

carpal complex resembling Australopithecus and H. habilis (Tocheri et al. , 2007 ), foot with primitive and unique attributes (Jungers et al. , 2009b ) and

a primitive shoulder complex, including a short clavicle and humerus with

little torsion (Larson et al. , 2007 , 2009 ). We investigate the proximal fem-

oral anatomy of LB1/9 in the context of this debate to assess whether the

morphology is consistent with that of a small-bodied modern human, or more

closely resembles those of other fossil hominins.

Methods

In order to account for size-related variation in proximal femur morphology,

we measured a large sample of great apes and humans. We sampled a wide

range of human populations including, from smallest to largest, Andaman

Islanders , African Pygmies , Pre-Dynastic Egyptians , European Americans ,

Inuit and African Americans , with a total of 130 individuals ( Table 13.1 ). The


great ape sample ( n = 154) also includes a wide size range, from Pongo and

Pan paniscus to Gorilla , that encompasses the fossil size range.

In addition to extant samples, the Orrorin tugenensis and H. fl oresiensis

femora (BAR 1002’00 and LB1/9, respectively) were compared to the fem-

ora of a number of extinct hominin taxa, including A. afarensis from Hadar

(Ethiopia), P. robustus from Swartkrans (South Africa), femora from Koobi

Fora (Kenya) attributed to P. boisei and early Homo , and the large femur

from Berg Aukas (Namibia) attributed to archaic Homo (Grine et al. , 1995 ;

Table 13.1 ). Measurements were collected on original specimens of all but the

Hadar femora, in which case measurements were taken on casts at Stony Brook

University and verifi ed against comparable measurements in the literature.

The variables are as follows (see also McHenry and Corruccini, 1978 ):

(1) Femoral head SI: the supero-inferior diameter of the femoral head.

(2) Femoral head AP: the anteroposterior diameter of the femoral head.

(3) Lesser troch–head: the minimum distance from the lesser trochanter to the

rim of the head.

(4) Neck height: the supero-inferior height of the femoral neck.

(5) Neck breadth: the anteroposterior breadth of the femoral neck.

(6) Biomechanical neck length: the distance from the lateral aspect of the

greater trochanter to the medial aspect of the femoral head, minus half of

femoral head SI (measurement 1, above).

Table 13.1. Extant and fossil samples.

Extant and fossil taxa Population/specimen #s n

Homo sapiens 130

Andaman Islanders 31

African Pygmies 18

Pre-Dynastic Egyptians 20

Inuit 20

African Americans 20

European Americans 21

Pan troglodytes 49

Pan paniscus 14

Gorilla gorilla 59

Pongo pygmaeus 32

Orrorin tugenensis BAR 1002’00 1

Australopithecus afarensis A.L. 288–1ap, A.L. 333–3 2

Paranthropus robustus SK 82, SK 97 2

? Paranthropus boisei KNM-ER 1503 1

early Homo KNM-ER 1472, 1481 2

Homo heidelbergensis Berg Aukas 1

Homo fl oresiensis LB 1/9 1


(7) Subtrochanteric AP: the anteroposterior diameter of the shaft just below

the lesser trochanter.

(8) Subtrochanteric ML: the medio-lateral diameter of the shaft just below the

lesser trochanter.

The lateral edge of the greater trochanter of BAR 1002’00 ( Orrorin ) is unfor-

tunately broken. We conservatively estimate that 2 mm is missing and add it to

the minimum measured value (72 mm) in which neck length is taken directly

to the broken lateral edge of the greater trochanter. Analyses that include the

minimum value do not differ qualitatively (i.e. BAR 1002’00 retains the same

nearest-neighbour relationships) from the analysis with the reconstructed bio-

mechanical neck length.

The geometric mean (GM, the n th root of the product of n measurements)

was selected because it faithfully preserves shape information when variables

(e.g. femoral head size) are assessed relative to the GM (Jungers et al. , 1995 ).

Proximal femur size was represented by the GM of all eight measurements.

Size is therefore based on the femoral measurements themselves rather than an

independent substitute for size that would be unavailable for most of the fossils

or have to be estimated for all with attendant confi dence intervals (e.g. body

mass). Each variable was divided by the GM to create size-adjusted, scale-free

‘shape’ variables, which then refl ect the relative size of each anatomical fea-

ture. Each shape variable was logged prior to entry into the multivariate ana-

lyses (Darroch and Mosimann, 1985 ).

Multivariate and bivariate analyses were conducted. A canonical variates

analysis (CVA) was performed using seven of the shape variables (relative

femoral head SI was omitted because it was identifi ed in the analysis as being

redundant with relative femoral head AP in that they co-vary so closely). Each

of the modern and fossil species were treated as separate groups, resulting in

12 groups (5 extant and 7 fossil species). Canonical variates analysis makes

the assumption that groups share equivalent variance/covariance structure,

and therefore assumes that the fossil hominin taxa (represented by small sam-

ple sizes) have the dispersion structures comparable to those of the modern

great ape and human taxa. Fortunately, CVA is relatively robust to violations

of these underlying assumptions. Canonical variates analysis differs from prin-

cipal components analysis in maximising between-group differences instead

of maximising variation among individuals (regardless of group membership)

in the entire sample. It also adjusts the between-groups distances relative to

the within-group variation, and plots individuals in this adjusted, Mahalanobis

distance space.

Bivariate analyses are performed with raw variables plotted against the GM.

Fossils are examined in scatter plots relative to reduced major axis (RMA)


regression lines through pooled, raw data as the relationships are expected to

be symmetric between variables (Smith, 2009 ).

Results

The results show that proximal femoral shape is distinct among various mod-

ern and fossil taxa, including early hominins. The CVA of proximal femur

shape completely separates modern humans from the great apes along the fi rst

axis, which accounts for 74.8% of the variation ( Figure 13.1a ). A principal

components analysis (not shown) produced very similar results. The key vari-

ables infl uencing CVA1 are a relatively large lesser trochanter-to-head distance

and small femoral head towards the right (great ape side) of the axis ( Table

13.2 ). To a lesser extent, small neck height and breadth are correlated with the

axis as well. Thus, human femora are characterised by relatively small lesser

trochanter-to-head distances, large femoral heads and, to a lesser degree, rela-

tively large neck diameters ( Figures 13.1 , 13.4 ).

Along axis one, the fossil hominin femora all fall towards the human dir-

ection relative to the great apes and, with a few exceptions (the Hadar and

Swartkrans specimens) fall outside the great ape range on this axis. Axis two

accounts for 16.2% of the variation and primarily separates orang-utan fem-

ora from those of other taxa; it is most strongly infl uenced by relatively large

femoral heads and small subtrochanteric shaft anteroposterior depths ( Figure

13.1a , Table 13.2 ), a combination that characterises orang-utan femora.

The femora of extinct hominins cluster together, mainly in the lower middle

portion of the plot ( Figure 13.1a ). The Turkana Basin (Kenya) femora attributed

to early Homo lie in the modern human shape space. There is some disparity in

shape between KNM-ER 1481 and KNM-ER 1472, but the difference is consist-

ent with the variation seen in modern taxa. While most authors interpret these

femora as representing the same taxon, some have interpreted the morphological

differences between these specimens as indicating that they belong to separate

taxa. Some of the apparent morphological difference (e.g. smaller head size of

KNM-ER 1472) is infl uenced by how one reconstructs damage to the specimen.

In light of this uncertainty, and the fact that the morphological difference can be

accommodated with intra-specifi c variation in modern taxa, we have no grounds

for rejecting the hypothesis that they belong to the same genus, early Homo .

Of particular note in the CVA analysis is the result that all the non- Homo

femora cluster together in a unique space outside of the range of human and,

with the exception of Swartkrans specimen SK97, great ape variation ( Figure

13.1a ). The Orrorin and H. fl oresiensis femora cluster with these early hominin

femora attributed to Australopithecus and Paranthropus .

6(a)

4

2

0

CV

2

–2

–4

–6 –4 –2

BAR 1002'00

KNM-ERBerg Aukas

1481

KNM-ER 1503

KNM-ER 1472A

KNM-WT 15000G

LB1/9 A.L. 333-3SK 97

H. sapiensP. troglodytesP. paniscusG. gorillaP. pygmaeus

O. tugenensisA. afarensisKNM-ER 1503

early HomoBerg AukasLB1/9

P. robustusSK 82A.L. 288-1ap

CV 1

0 2 4 6

6(b)

5

2

3

4

1CV

3

–1

0

–2

–3–4 –3 –2 –1 0

BAR 1002'00

Berg Aukas

KNM-ER 1503

KNM-ER 1472A

KNM-WT 15000GKNM-ER 1481

LB1/9

A.L. 333-3

SK 97




P. robustus

SK 82

A.L. 288-1ap

CV 2

1 2 3 4 5 6

Figure 13.1. Canonical variates analysis (CVA) based on seven proximal femur shape

variables. The fi rst two axes (a) show that humans, African apes and orang-utans are

distinct from one another in proximal femur shape. All the non- Homo femora cluster

together in a unique space outside the human and, with the exception of SK97, great

ape variation. The Orrorin and H. fl oresiensis femora cluster with these early hominin

femora. The third axis (b) further separates these early hominins (except A.L. 333–3)

from the modern taxa. Note that the Orrorin and H. fl oresiensis femora cluster with

these early hominin femora, and away from other fossil and modern Homo along this

axis, underscoring the primitive morphology in these taxa.


The third CVA axis (5.5% of variation) separates most of this early hominin

group from the remaining fossil and extant taxa, and is most strongly infl u-

enced (towards the top) by narrow neck breadth (AP), long biomechanical

neck length and large subtrochanteric ML diameter ( Figure 13.1b , Table 13.2 ).

The distinct femora (towards the top) include those attributed to Paranthropus

(SK 82, SK 97 and KNM-ER 1503) and A. afarensis (A.L. 288–1, but not A.L.

333–3) ( Figure 13.4 ). Once again, the Orrorin and H. fl oresiensis femora clus-

ter with this primitive, australopith group ( Figures 13.1b , 13.4 ).

The Mahalanobis D 2 distances further illustrate how much more similar the

Orrorin and H. fl oresiensis femora are to the australopith femora than they

are to any of the extant or other fossil femora ( Table 13.3 ). Distances between

all the extant taxa, and between extant and fossil taxa, differ signifi cantly

Table 13.2. Factor structure matrix of canonical variates analysis, with the most infl uential variables on the fi rst three roots shown in bold.

Shape variables Root 1 Root 2 Root 3

Femoral head AP –0.5209 0.7226 –0.0311

Lesser troch–head 0.6489 0.3259 –0.0887

Neck height –0.4420 –0.1299 0.2108

Neck breadth –0.3899 –0.2852 –0.6987

Subtrochanteric AP 0.2272 –0.5352 –0.1825

Subtrochanteric ML 0.2241 –0.2700 0.4879

Biomechanical neck length –0.2383 –0.3113 0.6179

% Variance explained 74.8 16.2 5.5

% Variance (cumulative) 74.8 91.0 96.5

Table 13.3. Mahalanobis D2 distances.

Taxon/specimen BAR 1002’00 LB1

Homo sapiens 31.97 25.62

Pan troglodytes 50.82 32.12

Pan paniscus 49.45 29.77

Gorilla gorilla 47.66 29.95

Pongo pygmaeus 67.92 51.31

BAR 1002’00 0 17.56

Australopithecus afarensis 16.64 12.06

Paranthropus robustus 18.04 10.89

KNM-ER 1503 13.04 8.65

early Homo 33.49 27.55

Berg Aukas 49.74 38.16

LB1 17.56 0


(F-statistic, p < 0.01) from one another. With respect to these shape variables,

BAR 1002’00 is most similar to KNM-ER 1503, the Hadar femora, LB1/9, and

the Swartkrans femora, followed distantly by modern humans and the early

Homo femora. LB1/9 similarly clusters most closely to KNM-ER 1503, the

Swartkrans femora, the Hadar femora, BAR 1002’00, followed more distantly

by modern humans and the remaining non-human groups ( Table 13.3 ).

Femoral head size is of special interest because it has been described as rela-

tively large in BAR 1002’00 (Pickford et al. , 2002 ), and there has been some

debate about allometric patterns in human femoral head size. When compared

against proximal femur size (the geometric mean of all eight measurements),

femoral head size in humans and orang-utans is greater than those of African

apes ( Figure 13.2 ). This is true even at the smallest overall proximal femoral

sizes, meaning that femoral size alone does not explain the relatively small

head size observed in Australopithecus , Paranthropus and H. fl oresiensis fem-

ora (or the large ones in orang-utans). The Orrorin femur has an intermediate

head size, greater than the typical size of African apes or australopiths, but less

Berg Aukas

KNM-WT 1503

RMA: y = 1.134x + 0.4245560

55

50

45

40

Hea

d di

amet

er (

mm

)

35

30

2520 25 30 35

Proximal femur size (geometric mean, mm)

40 45 50 55

KNM-ER 1472A

KNM-ER 1481

LB1/9

A.L. 288-1ap

A.L. 333-3

SK 97KNM-ER 1503

SK 82BAR 1002’00




P. robustus

Figure 13.2. Bivariate plot of head diameter and proximal femur size, with RMA line

fi t through all data. Femoral head size in humans and orang-utans is relatively greater

than those of African apes, even at the smallest sizes. Australopithecus , Paranthropus

and H. fl oresiensis femora have smaller heads than modern humans of comparable

size. The Orrorin femur (BAR 1002’00) has an intermediate head size, greater than

the typical size of African apes or australopiths, and less than most humans and

orang-utans. The H. fl oresiensis femur (LB1/9) has a relatively small head.


than most humans and orang-utans. However, its head size is within the intra-

specifi c range of either. The head sizes of KNM-ER 1472, KNM-ER 1481 and

KNM-WT 15000 are also intermediate, relatively larger than those of austra-

lopiths and within the range of comparably sized modern humans. The slightly

low positions of the early Homo femoral head sizes are infl uenced to some

extent by other variables (e.g. biomechanical neck length, shaft breadth) that

contribute to large proximal femur sizes for these specimens. The Berg Aukas

femoral head is larger than any in our extensive modern human sample, but has

a relative size expected for such a large femur.

Biomechanical neck length is one of the most infl uential variables separating

the early hominin femora from extant and other fossil femora in the multivari-

ate analysis ( Table 13.2 ). The proximal femur size adjustment in this analysis

yields similar results to previous studies that have noted the long femoral necks

of the femora from Hadar, Swartkrans and East Turkana specimen KNM-ER

1503 (e.g. Napier, 1964 ; Day, 1969 ; Lovejoy et al. , 1973 ). When plotted against

proximal femur size ( Figure 13.3 ), it is apparent that the most of the fossil

Berg Aukas

KNM-WT 15000G

RMA: y = 1.754x – 3.262690

80

70

60

50

Bio

mec

hani

cal n

eck

leng

th (

mm

)

40

3020 25 30 35

Proximal femur size (geometric mean, mm)

40 45 50 55

KNM-ER 1472A

KNM-ER 1481

LB1/9

A.L. 288-1ap

A.L. 333-3

SK 97

KNM-ER 1503SK 82

BAR 1002’00




P. robustus

Figure 13.3. Bivariate plot of biomechanical neck length and proximal femur size,

with RMA line fi t through all data. Most of the fossil hominin femora have long

necks, with some (e.g. KNM-ER 1503) exceeding the range of modern human

variation. The Orrorin femur has an unusually long neck, greater than that seen in

the two Hadar femora. Like A.L. 288–1, LB1/9 has a longer neck than expected for a

comparably sized modern human.


hominin femora have long necks, with some (e.g. KNM-ER 1503) exceeding

the range of modern human variation. In this regard, the Orrorin femur has

an unusually long neck, greater than that seen in the two Hadar femora. Like

A.L. 288–1 (but not A.L. 333–3), LB1/9 has a longer neck than expected for a

comparably sized modern human. KNM-ER 1481 and KNM-WT 15000G also

have unusually long necks, longer than that of KNM-ER 1472 and beyond the

modern human range. Berg Aukas has a neck length consistent with its mas-

sive size.

Biomechanical neck length, as measured in this and previous studies (e.g.

McHenry and Corruccini, 1978 ) from the lateral extent of the greater trochan-

ter, is infl uenced by the morphology of the greater trochanter. Modern human

and early Homo femora tend to have laterally projecting greater trochanters

( Figure 13.4 ; Harmon, 2009a ), but considerable variability exists. The lateral

extent of the greater trochanter increases the mechanical lever arm of the glu-

teal musculature, and this increased leverage is refl ected in the biomechanical

neck length measurement. In this regard, the lateral projection of the greater

trochanter in the Flores specimen LB1/9 contributes to its long neck in a man-

ner resembling femora of early Homo ( Figure 13.4 ), including KNM-ER 1481,

KNM-ER 1472 and KNM-WT 15000 from the Turkana Basin , and D4167

from Dmanisi, Georgia (Lordkipanidze et al. , 2007 ). The adaptive signifi cance,

if any, of the laterally-projecting greater trochanter is unknown, but could be

related to changes in the gluteal insertions (Harmon, 2009a ) or as a means of

maintaining a long gluteal lever arm without further lengthening the femoral

neck and subjecting it to more elevated bending moments. The long biomech-

anical neck (i.e. including trochanter projection) is associated with laterally-

fl aring ilia in australopiths (Lovejoy et al. , 1973 ) and H. fl oresiensis specimen

LB1 (Jungers et al. , 2009a ). Modern human femora have short biomechanical

neck lengths despite the lateral projection of the greater trochanter, likely asso-

ciated with relatively narrow iliac breadth (Ruff, 1995 ).

Discussion

The questions posed in this study concern what the femora of two new hominin

taxa, O. tugenensis and H. fl oresiensis , tell us about the evolution of the hip and

bipedal gait. The results clearly show that the Orrorin femur does not resemble

those of great apes, but rather resembles those of fossil hominins, supporting

the conclusions reached by Senut et al. ( 2001 ), Pickford et al. ( 2002 ) and Galik

et al. ( 2004 ). Results also show that the Orrorin femur resembles those of the

early hominins A. afarensis and Paranthropus more closely than femora of

fossil or modern Homo . Although BAR 1002’00 has a slightly larger femoral


head than in most early hominin femora, it shares the long, narrow (AP) neck

and broad (ML) shaft distinctive of Australopithecus and Paranthropus femora

( Figure 13.4 ). Therefore, its overall morphological similarity to the femora of

gracile and robust australopiths contrasts with Pickford et al. ’s ( 2002 ) char-

acterisation of the Orrorin femur as being more human-like than australop-

ithecines. This, in turn, confl icts with the phylogenetic hypothesis that Orrorin

is ancestral to Homo to the exclusion of the australopithecines (Senut et al. , 2001 ). Instead, the overall primitive hominin morphology of the Orrorin femur

is consistent with a phylogenetic hypothesis that it is a basal member of the

hominin clade, namely a sister taxon to a clade consisting of Australopithecus

and later hominins ( Ardipithecus and Sahelanthropus are not being consid-

ered here owing to a lack of comparable data). We believe this hypothesis to

be the most likely one, given current anatomical and geochronological evi-

dence. While the femora of Orrorin and gracile and robust australopiths are not

identical, and the possibility of homoplasy cannot yet be ruled out (Wood and

Harrison, 2011 ), the similarities among them point to phylogenetic and func-

tional affi nities (Richmond and Jungers, 2008 ).

Regarding the continuing debate over whether or not australopiths have rela-

tive small femoral heads, the results here suggest that they do, supporting con-

clusions reached by some (e.g. McHenry and Corruccini, 1976a , b ; Jungers,

1988 , 1991 ) but not others (e.g. Wolpoff, 1976 ; Ruff, 1998 ). Wolpoff ( 1976 )

criticised McHenry and Corruccini ( 1976a ) for assessing head size relative to

neck length and shaft breadth because the latter variables are large in austra-

lopiths and therefore are not suitable variables for size adjustment. However,

McHenry and Corruccini ( 1976a ) did include a multivariate analysis, in which

the australopiths were characterised by small femoral heads when all variables

were considered together. In our study, all the variables were used to construct

a proximal femur size measure that minimises the infl uence of any single vari-

able. Because size here incorporates all the variables, it is not surprising that

our results comparing femoral head size to proximal femur size concur with

those of McHenry and Corruccini ( 1976b ) in showing that australopiths have

relatively small femoral heads. While some have implied that small femoral

heads in the small-bodied australopiths relative to modern humans is a con-

sequence of positive allometry in femoral head size coupled with biomechan-

ical factors (Lovejoy et al. , 1973 ), others found positive allometry in human

females but not males (Corruccini and McHenry, 1978 ) and no evidence of

positive allometry in some human populations (Wood and Wilson, 1986 ).

Using a narrow allometric approach with small-bodied humans as comparative

specimens, femoral head size in Australopithecus was smaller than expected

(Jungers, 1988 , 1991 ). In his biomechanical analysis of Hadar specimen A.L.

288–1, Ruff’s ( 1998 ) body mass estimate derived from estimates of bi-iliac


breadth and stature led to the conclusion that A.L. 288–1’s femoral head may

not be unexpectedly small. However, this conclusion will remain a tentative

hypothesis until the effects of extrapolation, choice of line-fi tting techniques

and broad prediction intervals for estimated body mass are known. To be fair,

we also note that the aim of Ruff’s study was to assess the biomechanics of the

early hominin hip, not to address relative femoral head size in the context of

overall proximal femoral size and shape (as we do here). To help resolve the

issue of whether or not the femoral head size in A.L. 288–1 meets biomechan-

ical expectations, it would be interesting to see a comparable analysis to Ruff’s

with a larger sample of small-bodied humans that overlap in size with A.L.

288–1. Our analysis does not explicitly include body mass, but shows that rela-

tive to the proximal femur as a whole, femoral head size in Australopithecus

and Paranthropus is small relative to comparably sized humans ( Figure 13.3 ).

Narrow (AP) neck, small-medium head

(a) (b) (c)

(e) (f)

(d) (g) (h)

Long neck, broad shaft

Broad (AP) neck, large head,long total length

Short neck,narrow shaft

Figure 13.4. Femora of (a) P. troglodytes , (b) BAR 1002’00 (cast), (c) A.L. 288–1ap

(cast), (d) LB1/9, (e) KNM-ER 1503 (reversed), (f) SK 97 (reversed), (g) KNM-ER

1481 and (h) H. sapiens . The Orrorin and H. fl oresiensis femora are similar to the

femora attributed to Australopithecus and Paranthropus in having very narrow (AP)

necks, and relatively small-intermediate heads. These and the femora attributed to

early Homo (KNM-ER 1472, 1481) also have a relatively long neck and broad (ML)

shaft. The early Homo femora share with modern humans a broader neck, larger head

and (where known) a longer total length. Modern human femora have a short neck

and narrow shaft. In proximal femoral anatomy, neither Orrorin nor H. fl oresiensis

resemble fossil or modern Homo more closely than they resemble australopiths.


The results also show that the femoral anatomy of H. fl oresiensis is not

consistent with that of a modern human at small size. For example, some

of the Andaman Islanders and Pygmies have a comparable (a few even

smaller) proximal femur size to that of LB1/9, but LB1/9 has a smaller

femoral head and longer femoral neck ( Figures 13.2 and 13.3 ). In these

respects, the Flores specimen LB1/9 resembles Hadar specimen A.L. 288–1,

Turkana specimen KNM-ER 1481 and other early hominins ( Figures 13.2

to 13.4 ). The primitive morphology of the proximal femur is therefore not

explained by the small size of LB1/9. Researchers who argue that LB1 rep-

resents a diseased modern human (Weber et al. , 2005 ; Jacob et al. , 2006 ;

Martin et al. , 2006a , 2006b ; Richards, 2006 ; Hershkovitz et al. , 2007 ) need

to present evidence that the disease results in the development of primitive

hip anatomy in conjunction with a relatively small brain, and primitive anat-

omy of the brain, cranium (Argue et al. , 2006 ; Gordon et al. , 2008 ), wrist

(Tocheri et al. , 2007 ), shoulder (Larson et al. , 2007 ), foot (Jungers et al. , 2009b ), limb proportions (Morwood et al. , 2005 ; Jungers, 2009 ) and limb

bone robusticity (Jungers et al. , 2009a ). Our results instead support fi nd-

ings based on the morphology of these anatomical regions that LB1/9 and

other Liang Bua skeletal remains represent a distinct species likely sepa-

rated from the modern human lineage by a considerable amount of time. If

australopiths or early Homo had a unique pattern of bipedal gait (e.g. Stern

and Susman, 1983 ; Susman et al. , 1984 ), then the femoral anatomy and limb

robusticity and proportions suggest that H . fl oresiensis retained (or inde-

pendently evolved) a gait distinct from that of modern humans, including

the smallest people on Earth.

Conclusion

The results of this study show that the Orrorin femur more closely resem-

bles the femora of Australopithecus and Paranthropus than those of extant

great apes, or fossil or modern Homo . Its morphology is therefore not consist-

ent with it being characterised as more like human than australopith femora

(Pickford et al. , 2002 ) or a phylogenetic hypothesis that Orrorin is ancestral to

Homo to the exclusion of the australopithecines (Senut et al. , 2001 ). However,

its morphology is consistent with its age of 6 Ma, its taxonomic assignment

as a hominin and the functional conclusion that it was adapted for bipedalism

(Senut et al. , 2001 ; Pickford et al. , 2002 ). However, some aspects of fem-

oral neck cortical geometry (Kuperavage et al. , 2010 ), if confi rmed with more

reliable, higher resolution CT imaging (Ohman et al. , 2005 ; Richmond and

Jungers, 2008 ), may raise questions about hip function.


The proximal femoral anatomy of LB1/9 shows that it is not a small modern

human, and instead supports evidence from other anatomical regions that it

represents a distinct species, H. fl oresiensis , with strikingly primitive femoral

morphology.

Acknowledgements

We thank Sally Reynolds, Andrew Gallagher and Colin Menter for inviting

us and for their efforts and patience in organising the conference and edited

volume; Brigitte Senut and Martin Pickford for encouraging us to examine the

Orrorin fossils; and the curators of the museums housing the modern and fos-

sil specimens used in this study for their permission and hospitality. We also

thank Mike Morwood, Thomans Sutikna and numerous Indonesian colleagues

for their support and access to the Homo fl oresiensis fossils. We also thank

Henry McHenry, Osbjorn Pearson and the editors for valuable comments, and

acknowledge funding support from the George Washington University, Stony

Brook University, NSF-BCS 0521835 and the Australian Research Council.

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