Postcranial morphology of the middle Pleistocene humans from

Transcription

Postcranial morphology of the middle Pleistocene
humans from Sima de los Huesos, Spain
Juan Luis Arsuagaa,b,1, José-Miguel Carreteroc,a, Carlos Lorenzod,e,a, Asier Gómez-Olivenciaf,g,h,a, Adrián Pablosi,a,
Laura Rodríguezc,j, Rebeca García-Gonzálezc, Alejandro Bonmatía,b, Rolf M. Quamk,l,a, Ana Pantoja-Péreza,b,
Ignacio Martínezi,a, Arantza Aranburum, Ana Gracia-Téllezn,a, Eva Poza-Reya,b, Nohemi Salaa, Nuria Garcíaa,b,
Almudena Alcázar de Velascoa, Gloria Cuenca-Bescóso, José María Bermúdez de Castroj, and Eudald Carbonelld,e,p
a
Centro Mixto Universidad Complutense de Madrid - Instituto de Salud Carlos III de Evolución y Comportamiento Humanos, 28029 Madrid, Spain;
Departamento de Paleontología, Facultad Ciencias Geológicas, Universidad Complutense de Madrid, 28040 Madrid, Spain; cLaboratorio de Evolución
Humana, Departamento de Ciencias Históricas y Geografía, Universidad de Burgos, 09001 Burgos, Spain; dÀrea de Prehistòria, Departament d’Història i
Història de l’Art, Universitat Rovira i Virgili, 43002 Tarragona, Spain; eInstitut Català de Paleoecologia Humana i Evolució Social, 43007 Tarragona, Spain;
f
Departamento Estratigrafía y Paleontología, Facultad de Ciencia y Tecnología, Universidad del País Vasco–Euskal Herriko Unibertsitatea, 48080 Bilbao,
Spain; gIkerbasque, Basque Foundation for Science, 48013 Bilbao, Spain; hUMR 7194, CNRS, Département Préhistoire, Muséum National d’Histoire Naturelle,
Musée de l’Homme, 75016 Paris, France; iÁrea de Antropología Física, Departamento de Ciencias de la Vida, Universidad de Alcalá, 28871 Alcalá de Henares,
Spain; jCentro Nacional de Investigación Sobre la Evolución Humana, 09002 Burgos, Spain; kDepartment of Anthropology, Binghamton University, State
University of New York, Binghamton, NY 13902-6000; lDivision of Anthropology, American Museum of Natural History, New York, NY 10024-5192;
m
Departamento Mineralogía y Petrología, Facultad de Ciencia y Tecnología, Universidad del País Vasco–Euskal Herriko Unibertsitatea, 48080 Bilbao, Spain;
n
Área de Paleontología, Departamento de Geografía y Geología, Universidad de Alcalá, 28871 Alcalá de Henares, Spain; oPaleontología, Aragosaurus–
Instituto de Investigación en Ciencias Ambientales de Aragón and Facultad Ciencias, Universidad de Zaragoza, 50009 Zaragoza, Spain; and pInstitute of
Vertebrate Paleontology and Paleoanthropology of Beijing, 100044 Beijing, China
b
Current knowledge of the evolution of the postcranial skeleton in the
genus Homo is hampered by a geographically and chronologically
scattered fossil record. Here we present a complete characterization
of the postcranium of the middle Pleistocene paleodeme from the
Sima de los Huesos (SH) and its paleobiological implications. The SH
hominins show the following: (i) wide bodies, a plesiomorphic character in the genus Homo inherited from their early hominin ancestors;
(ii) statures that can be found in modern human middle-latitude populations that first appeared 1.6–1.5 Mya; and (iii) large femoral heads
in some individuals, a trait that first appeared during the middle
Pleistocene in Africa and Europe. The intrapopulational size variation
in SH shows that the level of dimorphism was similar to modern
humans (MH), but the SH hominins were less encephalized than Neandertals. SH shares many postcranial anatomical features with Neandertals. Although most of these features appear to be either
plesiomorphic retentions or are of uncertain phylogenetic polarity,
a few represent Neandertal apomorphies. Nevertheless, the full suite
of Neandertal-derived features is not yet present in the SH population. The postcranial evidence is consistent with the hypothesis based
on the cranial morphology that the SH hominins are a sister group to
the later Neandertals. Comparison of the SH postcranial skeleton to
other hominins suggests that the evolution of the postcranium occurred in a mosaic mode, both at a general and at a detailed level.
human evolution
phylogeny
Unfortunately, our understanding of the evolution and variation
of body size and shape in Pleistocene Homo before the Neandertals
is still quite limited due to a fragmentary and geographically and
chronologically scattered fossil record. This has resulted in contradictory views for certain specimens (see, for example, ref. 5 for
H. habilis). Most interpretations of body size and shape in early
Pleistocene Homo have relied on one specific individual: KNM WT15000 (6), which has heavily influenced the view that the wider, more
robust Neandertal bauplan was derived from and likely reflected
cold adaptation (7). Further studies (8, 9) and the discovery of additional fossil evidence (10, 11) support the idea that the original
reconstruction of the pelvis of KNM WT-15000, and thus a number
of the interpretations based on it, need to be reconsidered.
In the middle Pleistocene, very few individuals preserve partial
postcranial skeletons (12), and in most cases only fragmentary
Significance
The middle Pleistocene Sima de los Huesos (SH) fossil collection
provides the rare opportunity to thoroughly characterize the
postcranial skeleton in a fossil population, comparable only to that
obtained in the study of the Neandertal hypodigm and recent (and
fossil) modern humans. The SH paleodeme can be characterized as
relatively tall, wide, and muscular individuals, who are less encephalized than both Neandertals and modern humans. Some (but
not all) Neandertal derived traits are present, which phylogenetically links this population with Neandertals. Thus, the full suite of
Neandertal features did not arise all at once, and the evolution of
the postcranial skeleton could be characterized as following a
mosaic pattern.
| bauplan | postcranial anatomy | Sierra de Atapuerca |
D
ifferences in hominin adaptive strategies (1) are reflected in
the postcranial skeleton, and can be grouped into broad categories of body plan (or bauplans) (2), mainly reflecting hominin
posture and locomotion. The first of these may represent a partially
arboreal, facultative biped, if the genus Ardipithecus (and perhaps
Orrorin) is included within the hominins. The australopith bauplan
(present in both Australopithecus and Paranthropus) mainly reflects
terrestrial bipedalism, coupled with suspensory and climbing activities (3) that could have also been present in Homo habilis (4). In
more derived members of the genus Homo, the bauplan reflects an
obligate terrestrial bipedalism with reduced arboreal capabilities.
Within the genus Homo (excluding the enigmatic and insular species Homo floresiensis), different bauplans could be present among
early representatives, but among the more derived representatives
of the genus, two distinct bauplans can be differentiated based upon
the body breadth and overall robusticity, with Neandertals showing
a “wide” bauplan and modern humans showing a “narrow” bauplan.
www.pnas.org/cgi/doi/10.1073/pnas.1514828112
Author contributions: J.L.A., J.M.B.d.C., and E.C. codirected the Atapuerca excavations and research project; J.L.A. designed research; J.L.A., J.-M.C., C.L., A.G.-O., A.P.,
L.R., R.G.-G., A.B., R.M.Q., A.P.-P., I.M., A.A., A.G.-T., E.P.-R., N.S., N.G., A.A.d.V., G.C.-B.,
J.M.B.d.C., and E.C. performed research; J.L.A., J.-M.C., C.L., A.G.-O., A.P., L.R., R.G.-G.,
A.B., R.M.Q., A.P.-P., I.M., A.A., A.G.-T., E.P.-R., N.S., N.G., A.A.d.V., and G.C.-B. analyzed
data; and J.L.A., J.-M.C., C.L., A.G.-O., A.P., L.R., R.G.-G., A.B., R.M.Q., A.P.-P., and I.M.
wrote the paper.
Reviewers: T.W.H., Tulane University; and C.B.R., The Johns Hopkins University School
of Medicine.
The authors declare no conflict of interest.
Freely available online through the PNAS open access option.
1
To whom correspondence should be addressed. Email: jlarsuaga@isciii.es.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
1073/pnas.1514828112/-/DCSupplemental.
PNAS Early Edition | 1 of 6
ANTHROPOLOGY
Contributed by Juan Luis Arsuaga, July 29, 2015 (sent for review May 20, 2015; reviewed by Trenton W. Holliday and Christopher B. Ruff)
remains are found. Although middle Pleistocene populations have
been described as exceptionally robust (13), phylogenetic hypotheses are based mainly on the more abundant cranial sample (14, 15).
The recent analysis of 17 crania from Sima de los Huesos (SH)
points to a mosaic pattern of evolution in the cranium, with facial
modification being the first step in the evolution of the Neandertal
clade (16). The SH postcranial sample offers an unparalleled opportunity to assess both general aspects of body size and shape and
the detailed postcranial morphology, avoiding many of the problems associated with grouping geographically dispersed and chronologically disparate samples. The present study aims to clarify the
evolution of the body plan in the genus Homo based on the SH
postcranial collection, the largest ever found. We will characterize
the general body size and shape [stature, body breadth, body mass,
and encephalization quotient (EQ)] in the SH paleodeme within
the context of postcranial evolution in the genus Homo. In addition,
we focus in particular on whether the detailed morphological traits
found throughout the postcranial skeleton follow a mosaic pattern
of evolution, as seen in the crania, and whether there have been
changes in the Homo bauplan.
The SH Site
The Sima de los Huesos site is a well-known middle Pleistocene
site that has yielded more than 6,700 human fossils dated to c.
430 kiloyears (kyr) (16). All of the human remains come from the
LU-6 lithostratigraphic unit (17). At least 28 individuals of both
sexes and diverse ages at death (18) were preserved, fragmented,
and mixed with carnivore bones, mainly of Ursus deningeri (19).
These fossils have been considered phylogenetically related to the
Neandertals based on the skeletal morphology (14, 16, 20–22).
More than half of the sample corresponds to the postcranial
skeleton, with all anatomical parts represented, even the tiny distal
pedal phalanges.
The current postcranial minimum number of elements (after the
2013 field season) is 1,523, more than double the number published
15 years earlier (21) (SI Appendix, Table S1). Many of these fossils
are complete and for most elements at least one complete specimen
is preserved (10, 22–28). A minimum number of 19 individuals
based on the femora are represented in the SH postcranial sample,
including both immature and adult individuals.
All postcranial bones of the human skeleton are represented,
reducing the previous bias against some elements (thorax, hand,
and foot bones). This fact strongly suggests that complete human
bodies were deposited in SH (SI Appendix, Table S2 and Fig. S1).
This is consistent with previous hypotheses of an anthropic origin
for this accumulation (21).
General Body Size and Shape, Intrapopulational Variation,
and Encephalization
Stature. The mean stature of the SH hominins has been estimated based on 24 complete long bones from the upper and
lower limbs (26). The overall stature [(male mean + female mean)/2]
of the SH hominins (163.6 cm) is 3.0 cm taller than the mean
stature in Neandertals (160.6 cm) (SI Appendix, Table S3).
Body Mass. Body mass (BM) can be reconstructed from hominin
skeletal remains using both morphometric [stature and bi-iliac
breadth (BIB)] (29) or mechanical approaches (joint surface size of
weight-bearing skeletal elements) (30). The BM of one large male
(Pelvis 1 individual) calculated from stature and BIB is between
90.3 and 92.5 kg (25), and the Pelvis 2 individual seems to be slightly
broader (Fig. 1A). The pooled sex-weighted mean BM estimated
from five adult SH femoral heads is 69.1 kg and is 6.3 kg below the
Neandertal mean (75.4 kg) (SI Appendix, Table S4 and Fig. S2).
Body Shape. Evidence from the shoulder girdle, the thorax, and the
pelvis points to a wide and large body type in the SH hominins. The
SH clavicles are absolutely long compared with modern humans
(MH), and they show the type II curvature in the coronal plane
that is present in all pre-H. sapiens hominins (31). This character
has been related to a more lateral and higher position of the
scapulae (see below). Regarding the thorax, the absence of complete midthoracic ribs makes it difficult to assess whether
the size and shape of the SH costal skeleton is similar to that of
Neandertals (32). However, the dorsoventral size of the single
complete first rib is longer than MH and Neandertals, and an
Fig. 1. SH-selected measurements compared with other hominin groups. (A) Bi-iliac breadth. (B) Femoral total length. (C) Femoral head diameter.
(D) Femoral neck index (biomechanical length of the neck following ref. 60/femoral maximum length × 100). (E) Percentage of cortical area in the right and
left humeri and femora. (F) Palmar projection of the trapezium tubercle. EP1: 2.0–1.8 Mya early Pleistocene Homo; EP2: 1.7–0.8 Mya early Pleistocene Homo;
MP: non-SH middle Pleistocene Homo; Ne: Neandertals; MH: modern humans. See SI Appendix for raw data. Boxes: SD; whiskers: range.
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Arsuaga et al.
Intrapopulational Size Variation. Using a randomization method,
relying on bootstrapping, the size variation in the SH hominins
was studied as a proxy for their level of sexual dimorphism (33,
34), including additional anatomical parts that were previously
underrepresented (SI Appendix, Tables S5–S7). Contrary to previous suggestions that middle Pleistocene humans were more dimorphic (35, 36), the SH hominins do not show an unusual degree
of size variation compared with MH.
Different anatomical parts display different levels of variation with
between 6.1 and 98.2% of the samples of the same size randomly
generated from large samples of MH presenting more variation than
in SH. The variation observed in the different anatomical regions
may be due to differences in the SH sample sizes depending on the
skeletal region, variation in the different modern human samples
used, and/or varying correlation of the skeletal regions with overall
body size. Thus, sexual dimorphism in SH was not significantly different from the moderate level of sexual dimorphism exhibited by
MH. Although there appears to be a somewhat elevated level of
intrapopulational variation and sexual dimorphism in the SH sample
when we compare the BM values to that of modern humans (SI
Appendix, Table S4), this result is based on the still relatively small
sample of femoral head estimates (n = 5) in SH. In addition, modern
human sexual dimorphism shows some degree of populational variation, and future SH findings may allow for a more precise assessment of this matter.
EQ. Nine EQ values have been calculated for the SH adult crania
(16) using the femoral head diameter (FHD) to calculate BM (SI
Appendix, Table S8) and yield a mean EQ of 3.54. The higher EQ
of the SH population compared with the published values in the
early Pleistocene Dmanisi hominins (37) demonstrates that the
increase in brain size in SH was not simply a consequence of an
increase in body mass (29). Although the use of the FHD rather
than the BIB (see above) yields lower BM values and, consequently, higher EQ values, the EQ from the SH sample is still
significantly lower than that of Neandertals (P < 0.003) and MH
(P < 0.006). There is a further increase in the EQ in both MH
and Neandertals (SI Appendix, Table S8), which suggests that a
parallel encephalization process occurred after their last common ancestor (10). Nevertheless, the lower EQ value in the SH
population indicates that, in the case of the Neandertals, this
brain size increase occurred after the SH population.
Postcranial Skeletal Anatomy
The abundant postcranial record recovered from SH has allowed
for a detailed characterization of the skeleton of this paleodeme
and makes it possible to compare this sample with other Homo
populations (SI Appendix, Table S9).
Thorax and Spine. The dorsoventral size of the single SH complete
first rib and an incomplete second rib suggest that the SH
hominins had a larger costal skeleton relative to their stature
compared with MH (SI Appendix, Table S10 and Fig. S3). The
atlas displays a large maximum dorsoventral canal diameter
(related to the size of the foramen magnum of the SH crania).
The axis is craniocaudally low, and the atlantoaxial joint is
mediolaterally (ML) expanded (24). The SH hominins show C6
and C7 spinous processes that are more horizontally oriented
than in MH and shorter than in Neandertals. At least the L3 and
L5 lumbar vertebrae display very long and, unlike the Neandertals, dorso-laterally oriented transverse processes (Fig. 2A and
Arsuaga et al.
SI Appendix, Tables S11 and S12 and Figs. S3–S5). Finally, the SH
hominins show a reduced lumbar lordosis, i.e., a less curved lumbar
spine, based on the vertebral wedging in lumbar vertebrae and the
incidence of the pelvis, a derived feature shared with Neandertals
(25, 38).
Shoulder Girdle and Upper Limb. The SH glenoid cavity is consistently
taller and narrower (n = 10) than in MH, reflected in a low glenoid
index (SI Appendix, Fig. S6 and Tables S13–S16). The SH sample
shows a dominant dorsal position (n = 8) of the axillary sulcus for the
Musculus teres minor (on the axillary border), resembling the predominant condition in Neandertals. Only one specimen (Scapula IV)
displays a ventral sulcus (the most frequent condition in MH).
The curvatures of the SH clavicles in the transverse plane fall
within the normal variation in MH. Nevertheless, the curvatures
in the coronal plane, in all of the SH specimens where it can be
determined, are of type II, as is the case in all Neandertals that
we have studied and the few known early Pleistocene specimens.
In contrast, MH show three curvature types (31).
Most of the SH humeri display a consistent morphological
pattern that distinguishes them from MH and is similar to Neandertals. This pattern includes a transversely oval humeral
head, a projected and massive lesser trochanter, a narrower
deltoid tuberosity with two muscular crests, thick cortical diaphyses (Fig. 1E), a broader and deeper olecranon fossa, a relatively narrower medial distal pillar surrounding the olecranon
fossa (Fig. 2B), a rectangular and broader capitulum, and a
shallower trochlea with a less projecting lateral rim. In these two
latter traits, the specimens show some variation.
The ulnae have a broader olecranon process, an anterior
orientation of the trochlear notch (the plesiomorphic condition
for all hominins), a vertically extended radial notch, a short and
blunt supinator crest, a robust pronator crest, a blunt interosseous crest, a rounded and gracile diaphysis and pronounced
antero-posterior (AP) and ML shaft curvature (SI Appendix, Fig.
S7). This pattern is also present in the Neandertals and distinguishes them from MH (SI Appendix, Tables S13–S16).
Most of the SH radii (six of eight specimens) display a relatively
long and gracile neck, an antero-medially oriented radial tuberosity,
and a low robusticity index with a pronounced ML shaft curvature, as
in the Neandertals. However, two SH specimens show the relatively
short and robust neck, anteriorly oriented radial tuberosity, and the
straight and robust shaft typical of MH (SI Appendix, Fig. S8).
Hand. The SH hand is characterized by a strong development of the
palmar tubercles of the carpal bones associated with a deep carpal
tunnel (palmar projections of the tubercle of the trapezium and the
hamulus) (Fig. 1F); high mobility of the first metacarpal (MC1),
reflected in the saddle-shaped carpo-metacarpal articulation of the
thumb; high capacity for rotation of the second metacarpal (MC2);
robust thumbs with a strong attachment for the Musculus opponens
pollicis (Fig. 2C), relatively short proximal phalanges, and relatively
long distal phalanges; noncurved proximal and middle phalanges
with relatively broad trochleae; distal phalanges with expanded
distal tuberosities; pea-shaped pisiforms; and relatively short
(proximo-distal) lunates and relatively broad (radio-ulnar) triquetrals (SI Appendix, Table S17). The SH hand morphology indicates
a powerful precision grip and fine precision grasping capabilities
that are similar to what has been described in Neandertals (39) and
MH. In the SH hand, like in Neandertals, the powerful precision
grip is enhanced by the thumb robusticity and well-developed
flexor musculature.
Pelvic Girdle and Lower Limb. The SH pelvises are characterized
by their marked robusticity (e.g., large sacroiliac joint, iliac
tubercle, and ischial tuberosity) and large overall dimensions.
The SH sample shows remarkably broad, tall, and AP-expanded
pelvises. The total length of the sacrum and of the complete hip
bone, and of the ischium, ilium, and pubis, the vertical acetabular
ANTHROPOLOGY
incomplete second rib suggests that it was dorso-ventrally longer
than that of Kebara 2. This suggests that the SH hominins, like
Neandertals, had a larger costal skeleton relative to their stature
compared with MH (see below). Finally, this population presents
very broad elliptical pelves (Fig. 1A) characterized by very wide
sacra, pronounced lateral iliac flaring, and long pubic rami that
clearly separate it from the MH pelvic configuration (see below).
Fig. 2. SH-selected postcranial traits. (A) Third lumbar vertebra (L3). Cranial view of VL2, presenting a very long and dorso-laterally oriented transverse
process (arrowhead). (B) Humerus. Subadult (H-IV, Left) and adult (H-VI, Right) specimens showing the thin medial pillar and broad and deep olecranon fossa.
(C) First metacarpal (MC1). Palmar view of juvenile (AT-3104, Left) and adult (AT-5565, Right) specimens, both showing a strong attachment for the opponens
pollicis muscle (arrowheads). (D) Os coxae. Ventral view of AT-1000, displaying a strongly twisted anterior inferior iliac spine (white arrow) and a deep
iliopsoas groove (black arrow). (E) Femur. F-X (Left) and F-XI (Right) proximal femora in posterior view, showing a low neck angle, large gluteal ridges, and
well-developed hypotrochanteric fossae. Midshaft section (Middle, CT-scan image) is rounded and shows an absence of a pilaster. (F) Talus. Dorsal view of AT2803 that shows an expanded lateral malleolar facet (arrowhead) and parallel edges of the trochlea.
diameter, and the breadth of the ilium and sacrum are conspicuously above MH (SI Appendix, Table S18). The SH pelvic
remains are also distinct from MH in having an anteriorly located acetabulocristal buttress, a well-developed supraacetabular
groove and a thin and rectangular, plate-like superior pubic ramus that contrasts with the thick and stout pubis of MH (10, 25)
(SI Appendix, Figs. S9 and S10). These features, together with the
very broad elliptical pelvis, are shared with early and middle
Pleistocene Homo specimens, and they likely represent the plesiomorphic condition for the genus Homo.
Neandertals depart from the SH pattern mainly in having an
extreme craniocaudal flattening of the pubic ramus (10, 11, 25,
40). Neandertal pelvises, although broader than MH (probably
due to prominent iliac flaring), are narrower than SH, likely
related to a significantly smaller sacral breadth and iliac height in
Neandertals (SI Appendix, Table S18). Unlike MH, the anterior
inferior iliac spine (AIIS) of the Neandertals is medially twisted
relative to the anterior margin of the iliac blade and is bordered
by a deep iliopsoas groove that excavates the medial surface of
the AIIS (41, 42). This AIIS configuration agrees with that found
in the SH sample (Fig. 2D) and other middle Pleistocene hip
bones (43). In contrast, the iliopsoas groove in hip bones of
earlier Homo taxa is shallow and does not excavate the medial
surface of the AIIS (44).
The SH femora show the plesiomorphic morphological pattern
found in most earlier members of the genus Homo (45–47). The
SH femora have relatively longer and, on average, moderately
AP-flattened necks, ML-widened proximal (subtrochanteric) shaft,
relatively low-neck-shaft angle, large gluteal ridges, well-developed
hypotrochanteric fossae and proximal lateral crest, absence of a
true pilaster, very low point of minimum shaft breadth, and thicker
cortical bone than in MH (Figs. 1 D and E and 2E and SI Appendix,
Fig. S11 and Tables S19–S22).
The SH tibiae share a similar morphological pattern with Neandertals that includes large retroversion angle of the proximal
epiphysis (SI Appendix, Fig. S12 and Tables S19–S22), tibial condyles located in a more posterior position in relation to the axis of
the shaft, and flat proximal and distal articular surfaces. Distally,
there is moderate hypertrophy of the medial malleolus and presence of squatting facets in some adult specimens (25%), related by
some researchers to a hyperdorsiflexion of the ankle joint (48). The
robusticity of the fibula overlaps the upper range for MH.
In all of the anatomical details of the upper and lower limb,
the SH immature individuals follow the same pattern as in the
adult specimens (SI Appendix, Tables S14 and S20).
Foot. Despite subtle variation in Pleistocene hominin tali, some
consistent morphological variants can be identified among different
fossil samples (27, 49). The Neandertal talus displays broader lateral
malleolar facets (50) and talar heads compared with MH. In the SH
specimens, the peroneal facet is significantly broader (Fig. 2F) and
the talar head narrower than both Neandertals and MH (SI Appendix, Table S23). In SH, as in Neandertals, the trochlea is relatively broad with parallel sides, compared with the relatively narrow
Arsuaga et al.
Discussion
Implications for Evolution of Body Size and Shape. The SH hominins
could be included within the “wide Homo” bauplan due to their
absolutely and relatively large and ML-wide biotype consisting of a
large thorax with broad shoulders and pelvises, above-mediumheight body, thick bones, and great musculature and body mass.
This body shape is also largely present in other early and middle
Pleistocene individuals and in Neandertals. We base this hypothesis
on the Jinniushan pelvis (12) as well as on the similarity of the SH
coxal bone with KNM-ER 3228, OH28, Arago 44, and Kabwe
E.719 (53). Our analysis suggests that three aspects of this biotype
(body breadth, stature, and weight) show a mosaic pattern of
evolution (Fig. 1 A–C and SI Appendix, Table S24) (54, 55).
Although there are no known pelvic remains attributed to
H. habilis, in our view, a ML relatively wide biotype was likely
present (as the most parsimonious interpretation) in the earliest
members of the genus Homo and was inherited from their early
hominin ancestors. Variation in this width within the genus Homo
has been proposed to follow a latitudinal cline, similar to that
present in modern humans (56). This great width of the pelvis may
also have had obstetric implications, including a nonrotational delivery (56, 57). However, in SH Pelvis 1 the AP diameters of the
pelvic canal are similar or even larger than in modern males, and a
rotational delivery has been proposed (10, 25).
About 1.6–1.5 Mya some individuals began to show an increase in
stature, reaching heights comparable to those present in middlelatitude MH populations. Direct evidence, based on femoral head
size, of heavier bodies appears later, during the middle Pleistocene
(including the SH population) and is retained in Neandertals. Body
mass estimations based on other parameters such as the BIB-stature
or cortical thickness, as well as the size and shape of some African
femoral and pelvic remains (KNM-ER 736, 737, 1808, 3228, KNMWT 15000, OH 28, and 34) suggest that tall and heavy bodies were
present even earlier. Thus, the bauplan in the genus Homo seems to
have been characterized by a long period of stasis during which the
“wide” (with respect to their stature) body plan shared by different
Homo species (including the SH hominins) varied rather little
throughout the Pleistocene until the appearance of the new “narrow” bauplan in H. sapiens (10, 25, 26). The appearance of this
“narrow” bauplan has energetic implications, which have been invoked as one of the reasons for the success of our species (58),
although the major change in relative skeletal strength (lower-limb
diaphyseal cross-sectional geometry) within Homo may have taken
place after, not at, the origin of H. sapiens (59).
Pattern of Evolution of the Postcranial Anatomical Traits. The preservation of all anatomical parts in SH has allowed a detailed
characterization of the postcranial anatomy and has revealed that
the SH hominins share many anatomical features with Neandertals not present in MH. These could be Neandertal specializations,
but the scant fossil record of postcranial elements in early Pleistocene
Homo makes it difficult to establish a clear cladistic polarity for
many anatomical features, such as the morphology of the axis, the
proximal humerus, the ulna, or the tibia. Some traits whose polarity can be established seem to be mainly plesiomorphic
Arsuaga et al.
retentions in the SH hominins because they are already present in
earlier Homo specimens, such as the general morphology of the
pelvis and femur or the talar trochlea. Therefore, these traits do
not phylogenetically relate the SH population with Neandertals.
A few features that have been considered Neandertal-derived
traits are also present in the SH hominins, including a low degree of
lumbar lordosis, broad distal tuberosities of the manual phalanges,
and the wide bases of the lateral metatarsals (MTIII–V), which is
consistent with the hypothesis, based on the cranial morphology, that
the SH hominins are a sister group to the later Neandertals (16).
In addition, there are some Neandertal specializations that are
not present in the SH hominins, such as the lateral orientation of
the lumbar transverse processes, the less saddle-shaped carpometacarpal articulation of the thumb, and the extremely thin,
plate-like superior pubic ramus. Finally, some taxonomically
relevant traits are polymorphic in SH, although the Neandertal
condition is dominant. These features include, among others, the
general radius morphology (neck length, radial tuberosity orientation, and diaphyseal curvature), the morphology of the axillary border of the scapula, and the shape of the distal humerus.
The presence of these polymorphisms in the SH sample and their
fixation in the Neandertals suggests that a subsequent loss of
variation occurred in the latter.
The detailed postcranial anatomy in SH indicates that some of the
potentially derived Neandertal features were not yet present in this
population. Thus, the full suite of Neandertal features did not arise
all at once, and the evolution of the postcranial skeleton could be
characterized as following a mosaic pattern. A mosaic pattern was
also documented in the SH cranium (16) although, in this case, the
Neandertal suite of derived features forms a single functional
complex.
Conclusions
In general, the body plan in the genus Homo has been largely
characterized by stasis since ∼1.6 Mya until the appearance of
MH (2). Individuals with tall, wide, and heavy bodies, compared
with earlier hominins, were already present at this early date in
Africa and (probably) Asia. A subsequent slight increase in body
mass occurred only approximately 1 million years later in middle
Pleistocene populations (including SH), and these body parameters were largely maintained in the Neandertals. Variation in
body breadth in Pleistocene Homo has been suggested to follow
a latitudinal cline. Absolute and relative brain size increased
between the early and the middle Pleistocene, as seen in the
higher EQ in SH. This was followed by a subsequent further
increase in the EQ in Neandertals and MH.
In sum, SH offers the best proxy for the general postcranial size
and shape of Homo for at least the past 1 million years until the
appearance of MH. Despite large periods of morphological stasis
in the general body plan, the anatomical details of the postcranial
skeleton, as revealed in the SH sample, offer the best evidence for
a pattern of mosaic evolution in the postcranium within the
Neandertal lineage.
Materials and Methods
The SH postcranial sample up to the 2013 field season is composed of 1,523
elements (SI Appendix, Table S1). The comparative material used in this study is
listed in SI Appendix, Table S25. Additional information on materials can be
found in SI Appendix. To avoid methodological problems in estimating body
size parameters in the genus Homo, we have generally used the raw values for
femoral length, BIB, and FHD as proxies for stature, body breadth, and weight
in our comparisons with other fossils (Fig. 1). Additional information on the
materials and methods for stature, body mass, intrapopulational size variation,
and encephalization quotient can be found in SI Appendix).
ACKNOWLEDGMENTS. We thank our companions in the Atapuerca research
and excavation team; M. C. Ortega for her extraordinary and patient restoration of the fossils; A. Esquivel for his invaluable dedication to the ongoing
work at the SH site; J. Trueba for graphic documentation of the SH fossils
and fieldwork under very demanding conditions; and the following individuals
ANTHROPOLOGY
and wedge-shaped trochlea of MH (27, 49) (Fig. 1F). Finally, all
Pleistocene (non-H. sapiens) fossil tali, including SH, show a tall
trochlea compared with recent MH, allowing for a greater capacity
for dorsiflexion and plantarflexion of the ankle joint (51).
The calcanei of Neandertals are broad with a projected sustentaculum tali and a long calcaneal tuber (39). In SH, the calcanei are
also broad and the sustentaculum tali is even more projected (28).
The metatarsals from SH, Neandertals, and MH are very similar
except for the broader base of the lateral metatarsals (MTIII–V), a
potentially derived character shared between SH and Neandertals
(49). The SH proximal pedal phalanges present hypertrophy of the
shaft, and the distal phalanx of the big toe shows an expanded
distal tuberosity, as in the Neandertals (39, 52).
and their institutions for access to the modern and fossil comparative materials: P. Mennecier and A. Froment (Muséum National d’Histoire Naturelle);
B. Maureille and C. Couture (Université de Bordeaux 1); Y. Haile-Selassie,
B. Latimer, and L. Jellema (Cleveland Museum of Natural History); R. G.
Franciscus (University of Iowa); Y. Rak (for MH data) and I. Hershkovitz
ski (Natural History Mu(Tel Aviv University); C. B. Stringer and R. Kruszyn
seum, London); I. Tattersall (American Museum of Natural History); D.
Lieberman (Harvard University); R. Potts and M. Tocheri (Smithsonian Institution); J. Radovčic (Croatian Natural History Museum); R. W. Schmitz
(LandesMuseum Bonn); E. Cunha and A. L. Santos (Coimbra University);
and A. Marcal (Bocage Museum) and T. Holliday (Tulane University). Field
work at the Sierra de Atapuerca sites is supported by the JCYL and Fundación Atapuerca. Thanks also to Residencia Gil de Siloé; Ministerio de Economía y Competitividad (project CGL2012-38434-C03-01/02/03); Junta de
Castilla y León (project BU005A09); Direcció General de Recerca 2014 SGR899; and the European Social Fund. This research received support from
the SYNTHESYS Project www.synthesys.info/, which is financed by European
Community Research Infrastructure Action under the FP7 integrating Activities Programme. A.G.-O. was supported by a Marie Curie Intra-European
Fellowships research fellowship during part of this work and by the research
group IT834-13 (Eusko Jaurlaritza/Gobierno Vasco); A.G.-T. was supported by
a contract grant from Ramón y Cajal Program (RyC-2010-06152); A.B., L.R.,
R.G.-G., A.P.-P., A.A.d.V., and N.S. received grants from Fundación Atapuerca;
R.M.Q. received financial support from Binghamton University (SUNY) and the
American Museum of Natural History; E.P.-R. was supported by a Comunidad
Autónoma de Madrid Grant S2010/BMD-2330; and L.R. by a contract grant
from Consejería de Educación de la Junta de Castilla y León and the European
Social Fund (CPIN. 03-461AA-692.01).
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POSTCRANIAL MORPHOLOGY OF THE MIDDLE PLEISTOCENE HUMANS
FROM SIMA DE LOS HUESOS, SPAIN.
Authors: Juan-Luis Arsuagaa,b,1, José-Miguel Carreteroc,a, Carlos Lorenzod,e,a, Asier
Gómez-Olivenciaf,g,h,a, Adrián Pablosi,a, Laura Rodríguezc,j, Rebeca García-Gonzálezc,
Alejandro Bonmatía,b, Rolf M. Quamk,l,a, Ana Pantoja-Péreza,b, Ignacio Martínezi,a,
Arantza Aranburum, Ana Gracia-Téllezn,a, Eva Poza-Reya,b, Nohemi Salaa, Nuria
Garcíaa,b, Almudena Alcázar de Velascoa, Gloria Cuenca-Bescóso, José-María Bermúdez
de Castroj, Eudald Carbonelld,e,p.
Author’s Affiliations:
a
Centro Mixto UCM-ISCIII de Evolución y Comportamiento Humanos. Avda. Monforte
de Lemos, 5. 28029 Madrid, Spain.
b
Dpto. de Paleontología. Fac. Ciencias Geológicas. Universidad Complutense de
Madrid, Avda. Complutense s/n, 28040 Madrid, Spain.
c
Laboratorio de Evolución Humana, Dpto. de Ciencias Históricas y Geografía,
Universidad de Burgos, Edificio I+D+i, Plaza Misael Bañuelos s/n, 09001 Burgos,
Spain.
d
Àrea de Prehistòria, Dept. d’Història i Història de l’Art, Univ. Rovira i Virgili, Av.
Catalunya, 35, 43002 Tarragona, Spain.
e
Institut Català de Paleoecologia Humana i Evolució Social, C/ Marcel·lí Domingo s/n
(Edifici W3), Campus Sescelades, 43007 Tarragona, Spain.
f
Dept. Estratigrafía y Paleontología, Facultad de Ciencia y Tecnología, Universidad del
País Vasco-Euskal Herriko Unibertsitatea. Apdo. 644, 48080 Bilbao, Spain.
g
IKERBASQUE. Basque Foundation for Science, 48013 Bilbao, Spain.
h
UMR 7194, CNRS, Dépt. Préhistoire, Muséum national d'Histoire naturelle. Musée de
l’Homme, 17, Place du Trocadéro, 75016 Paris, France.
i
Área de Antropología Física, Depto. de Ciencias de la Vida. Universidad de Alcalá,
28871 Alcalá de Henares, Spain.
j
Centro Nacional de Investigación sobre la Evolución Humana, Paseo Sierra de
Atapuerca, 09002 Burgos, Spain.
k
Dept. of Anthropology, Binghamton University (State University of New York),
Binghamton, NY 13902-6000, USA.
l
Division of Anthropology, American Museum of Natural History, New York, NY 10024-
5192, USA.
m
Departamento Mineralogía y Petrología, Facultad de Ciencia y Tecnología,
Universidad del País Vasco-Euskal Herriko Unibertsitatea. Apdo. 644, 48080 Bilbao,
Spain.
n
Área de Paleontología. Depto. de Geografía y Geología. Universidad de Alcalá, 28871
Alcalá de Henares, Spain.
o
Paleontología,
Aragosaurus-IUCA
and
Facultad
Ciencias,
Universidad
de
Zaragoza,50009 Zaragoza, Spain.
p
Visiting Professor, Institute of Vertebrate Paleontology and Paleoanthropology of
Beijing, 100044 China.
1
Corresponding author: Juan-Luis Arsuaga, Centro Mixto Universidad Complutense de
Madrid - Instituto de Salud Carlos III (UCM-ISCIII) de Evolución y Comportamiento
Humanos, c/ Monforte de Lemos 5 – Pabellón 14, 28029 Madrid (Spain). Telephone:
+34918222834. Email: jlarsuaga@isciii.es
1-SKELETAL REPRESENTATION
Table S1. Complete inventory of SH postcranial
each element
Minimum Number of
Elements (MNE)
AD
SubAD Indet Total
M F ?
Total vertebrae
212
Cervical V.
28
28
14
70
Thoracic V.
46
49
95
Lumbar V.
19
28
47
58
58
2
Total ribs
118
Manubria
4
3 2 4
11
Clavicles
20
6
2
6
13
Scapulae
27
8 2 2
12
Humeri
24
7 3 4
11
Radii
25
6 3 4
12
Ulnae
25
Carpal bones
131
Scaphoid
14
5
19
Lunate
14
7
21
Triquetral
10
6
16
Pisiform
6
3
9
Trapezium
13
3
16
Trapezoid
13
4
17
Capitate
14
5
19
Hamate
10
4
14
Metacarpals
63
Mtc I
6
12
18
Mtc II
9
3
12
Mtc III
7
3
10
Mtc IV
3
3
6
Mtc V
11
6
17
Hand phalanges
325
Proximal
68
39
19 126
Middle
50
34
11 104
Distal
59
33
3
95
17
4
Innominate bones 5 5 4
31
2
3
5
Sacra
10
5
3
Coccygeal V.
8
6 2 1
23
Femora
32
4 2 5
5
Patellae
16
5 2 3
13
Tibiae
23
1 1 7
9
Fibulae
18
Tarsal bones
130
Talus
21
3
24
remains and MNI represented by
Minimum Number of Individuals
(MNI)
AD
SubAD Indet
Total
M F ?
12
5
2
5
12
3
3
2
3
1
2
3
6
6
7
8
5
8
8
6
3
8
8
8
7
5
4
4
3
2
2
3
4
3
4
4
2
6
7
2
3
2
3
7
6
7
3 1 1
2
3
2
4 1
2 2 3
4 2
1 1 3
5
10
5
2
14
3
7
3
3 4 4
3
2
5
5
3
3
1
2
1
2
3
1
2
7
4
11
16
14
15
14
13
13
12
10
6
10
10
11
11
10
10
6
7
4
9
13
13
12
17
10
4
19
10
13
8
14
14
Calcaneus
Navicular
Cuboid
Medial cuneiform
Inter. cuneiform
Lateral cuneiform
Metatarsals
Mtt I
Mtt II
Mtt III
Mtt IV
Mtt V
Foot phalanges
Proximal Ph. I
Distal Ph. I
Proximal II-V
Middle II-V
Distal II-V
17
20
15
9
13
9
9
5
3
5
2
3
10
7
6
5
5
5
1
4
4
4
10
10
9
7
20
35
52
16
53
9
Total MNE
9
26 4 3 2
6
25
9
5
18
7
3
14
5
3
15
8
2
12
5
1
51
15
6
5
8
4
1
10
5
3
9
4
3
9
4
3
230
20
8
8
16
5
4
64
68
62
1523
Final MNI
M = male; F = female; AD = adult; SubAD = subadult
15
14
10
8
10
6
11
11
5
8
7
7
16
16
9
19
Table S2. Relative representation and cumulative percentage
Anatomical Units (AU)
1. Neurocrania
2. Mandibles
3. Dentition
4. Cerv. vertebrae
5. Thor. vertebrae
6. Lumb. vertebrae
7. Sacra
8. Ribs
9. Claviculae
10. Scapulae
11. Prox. humeri
12. Humeral shafts
13. Dist. humeri
14. Prox. ulnae
15. Ulnar shafts
16. Dist. ulnae
17. Prox. radii
18. Radial shafts
19. Dist. radii
20. Carpals
21. Metacarpals
22. Hand phalanges
23. Innominate bones
24. Prox. femora
25. Femoral shafts
26. Dist. femora
27. Patellae
28. Prox. tibiae
29. Tibial shafts
30. Dist. tibiae
31. Prox. fibulae
32. Fibular shafts
33. Dist. fibulae
34. Tali
35. Calcanei
36. Ant. tarsals
37. Metatarsals
38. Foot phalanges
TOTAL
NºAU
17
20
533
70
95
47
10
118
20
27
18
37
27
22
27
10
24
32
20
131
63
325
31
35
36
22
16
18
35
19
10
20
19
24
26
84
51
230
2369
One
Relative
MNAU
Skeleton
MNAU
1
1
32
7
12
5
1
24
2
2
2
2
2
2
2
2
2
2
2
16
10
28
2
2
2
2
2
2
2
2
2
2
2
2
2
10
10
28
233
17.0
20.0
16.7
10.0
7.9
9.4
10.0
4.9
10.0
13.5
9.0
18.5
13.5
11.0
13.5
5.0
12.0
16.0
10.0
8.2
6.3
11.6
15.5
17.5
18.0
11.0
8.0
9.0
17.5
9.5
5.0
10.0
9.5
12.0
13.0
8.4
5.1
8.2
431.2
3.9
4.6
3.9
2.3
1.8
2.2
2.3
1.1
2.3
3.1
2.1
4.3
3.1
2.6
3.1
1.2
2.8
3.7
2.3
1.9
1.4
2.7
3.6
4.1
4.2
2.6
1.9
2.1
4.1
2.2
1.2
2.3
2.2
2.8
3.0
1.9
1.2
1.9
100
Cumulative
% MNAU
3.9
8.5
12.4
14.7
16.5
18.7
21.0
22.1
24.4
27.5
29.6
33.9
37.0
39.6
42.7
43.9
46.7
50.4
52.7
54.6
56.0
58.7
62.3
66.4
70.6
73.2
75.1
77.2
81.3
83.5
84.7
87.0
89.2
92.0
95.0
96.9
98.1
100.0
2048.9
MNAU = minimum number of anatomical units = number of bones or bone
portions preserved in a sample divided by number of that bone or bone portion in a
complete skeleton.
Figure S1. Cumulative percentage of the minimum number of anatomical units
(MNAU), i.e., number of bones or bone portions preserved in a sample divided by
number of that bone or bone portion in a complete skeleton. 1. Neurocrania; 2.
Mandibles; 3. Dentition;4. Cerv. vertebrae; 5 Thor. vertebrae; 6. Lumb. vertebrae; 7.
Sacra; 8. Ribs; 9. Claviculae; 10. Scapulae; 11. Prox. humeri; 12. Humeral shafts; 13.
Dist. humeri; 14. Prox. ulnae; 15. Ulnar shafts; 16. Dist. ulnae; 17. Prox. radii; 18.
Radial shafts; 19. Dist. radii; 20. Carpals; 21. Metacarpals; 22. Hand phalanges; 23.
Innominate bones; 24. Prox. femora; 25. Femoral shafts; 26. Dist. femora; 27. Patellae;
28. Prox. tibiae; 29. Tibial shafts; 30. Dist. tibiae; 31. Prox. fibulae; 32. Fibular shafts;
33. Dist. fibulae; 34. Tali; 35. Calcanei; 36. Ant. tarsals; 37. Metatarsals; 38. Foot
phalanges.
2- GENERAL BODY SIZE AND SHAPE, INTRAPOPULATION VARIATION
AND ENCEPHALIZATION
2.1-STATURE
Systematic work at the Sima de los Huesos has allowed us to reconstruct 27 complete
long bones. Despite the methodological difficulties involved in the estimation of stature
in fossil humans (i.e. bone type, body proportions, sex assignment, statistical
techniques, etc.) and the lack of consensus on a valid method broadly applicable in all
cases, we have used the multiracial and combined-sex formulae proposed by Sjøvold (1)
to estimate the mean stature of the SH hominins based on 24 complete long bones
(excluding the fibula) (2).
Although the differences between the SH and Neandertal samples are not significant, it
is likely that the SH hominins were somewhat taller on average than the Neandertals
since the SH hominins had, on average, longer limb bones than the Neandertals (2).
The SH male and female means fall in the category of ‘above medium height’ and ‘tall
height’ individuals defined by Martin and Saller (3) for recent H. sapiens. The same
average in Neandertals falls more clearly into the category of ‘medium height’
individuals. However, in both samples ‘tall’ individuals, (i.e., above 170 cm for men and
160 cm for women) can be found. In light of our results, it seems that early and middle
Pleistocene humans from Africa, Asia, and Europe were characterized by heights in the
range of Medium and Above-Medium individuals, although tall individuals are found in
all three geographical areas. During the late Pleistocene, Neandertals reduced their
height only slightly compared with their ancestors such as the people from Sima de los
Huesos. As noted previously by others, the earliest H. sapiens populations (Skhul and
Qafzeh) had a radically different stature from earlier humans (177.4 cm pooled sex
mean).
Table S3. Comparison of mean stature for three fossil Homo samples
Sima de los Huesos
Neandertals
Early modern humans
Mean
SD
n
Mean
SD
n
Mean
SD
n
Males
169.5
4.0
19
166.7
5.9
26
185.1
7.1
11
Females
157.7
2.0
5
154.5
4.6
13
169.8
6.5
6
Pooled sex
mean(a)
163.6
160.6
177.4
SD = standard deviation; n = sample size. Stature in cm.
Early modern humans from Skhul and Qafzeh [see Table S25 and Carretero et al. (2)].
(a) Pooled sex mean = (male bones mean + female bones mean)/2.
2.2-BODY MASS
Among the SH sample, the body mass for the complete male Pelvis 1 (4), has been
estimated elsewhere as between 90.3 and 92.5 kg (5). However, in order to be consistent
in our comparisons between the SH hominins and Neandertals, we have estimated the
body mass (BM) based on femoral head size in both samples (Table S25). Since these
humans are known to be large bodied (4, 6), we used Grine et al.’s formula (7) for BM
estimation, following Auerbach and Ruff’s recommendations (8).
We have calculated a weighted mean of body mass estimations for both SH and
Neandertals. This takes into account the variation within each body mass estimate, i.e.,
the standard deviation for each individual prediction, SDx, using a meta-analysis
approach. To calculate SDx the following equation was used from Etxeberria (9).
SDX=Y'0/(Se √(1+1/n0))
where Y'0 is the predicted value, Se is the standard error of the estimate and n is the
number of observations. Individual and mean ranges for SH and Neandertals are shown
in Figure S2.
Table S4. Individual body mass estimates for several SH femoraa and the weighted
mean of the SH sample and Neandertals
95%
Femoral head
Sample/specimen
Sex
Body mass Confidence
diameter
interval
SH F-XI
Female
41.8
58.3
F-XVI
F-XII
F-XIII
F-X
Mean SH
Female
Male
Male
Male
Pooled sex weighted
mean
Male weighted mean
Neandertals
(N=14)
a
Female weighted
mean
Pooled sex weighted
mean
Male weighted mean
Female weighted
mean
41.2
49.0
48.3
52.8
56.9
74.6
73.0
83.3
69.1
59.1-79.0
76.8
70.7-82.9
57.6
52.9-62.3
72.1
67.0-77.2
76.3
71.6-81.0
61.6
56.0-77.2
Using Grine et al.’s (7) formula: 2.268*FH-36.5 (r=0.92; SEE=4.3).
Femoral head diameter in mm, body mass in kg.
The population weighted mean and 95% confidence interval was obtained from the
meta-analysis.
Neandertal sample: Males = La Ferrassie 1, Spy 2, Neandertal 1, La Chapelle-aux-Saints 1,
Amud 1, Kebara 2, Krapina 213, Le Moustier 1, Krapina 207 and Krapina 208. Females =
Tabun C1, La Ferrassie 2, Sima de las Palomas and Krapina 214. See also Figure S2.
Figure S2. Forest plot of body mass estimations through each femur and the weighted group mean. Amud 1; Ke2=Kebara 2; Krap207=Krapina
207; Krap208=Krapina 208; Krap213=Krapina 213; Krap214=Krapina 214; LCH= La Chapelle-aux-Saints 1; LF1=La Ferrassie 1; LF2=La
Ferrassie 2; LM= Le Moustier 1; NEA=Neandertal 1; SdP=Sima de las Palomas; SP2=Spy 2; TC1=Tabun C1.
The area of each square is proportional to the weight of each individual’s body mass in the meta-analysis (those estimations with larger SDx are
weighted less in the analysis). The horizontal lines represent the confidence intervals (95%) for each individual’s body mass estimation.
2.3-SIZE VARIATION AND SEXUAL DIMORPHISM
Table S5. Variables used in the size variation analysis
Anatomical
Variables
Details
Region
Endocranial capacity
in cubic centimeters
Cranium
Mandibular corpus at
= (mandibular corpus height × mandibular
Mandible
mental foramen
corpus breadth at mental foramen)1/2
geometric mean
Glenoid fossa geometric = (glenoid fossa height × glenoid fossa
Scapula
mean
breadth)1/2
Proximal epiphysis
= (proximal epiphysis breadth × head
Humerus
geometric mean
vertical diameter × head transverse
diameter)1/3
Midshaft perimeter
Biepicondylar breadth
Proximal epiphysis
= (olecranon breadth × coronoid breadth ×
Ulna
geometric mean
olecranon height × trochlear
anteroposterior diameter × coronoid
height)1/5
Proximal perimeter
Midshaft perimeter
Proximal epiphysis
= (mediolateral diameter of the radius head
Radius
geometric mean
× anteroposterior diameter of the radius
head)1/2
Neck perimeter
Distal breadth
Atlas superior transverse
Vertebrae
diameter
Axis superior transverse
diameter
L5 Vertebral body
= (dorsoventral diameter × transverse
geometric mean
diameter)1/2
Lumbosacral surface
= (transverse diameter × anteroposterior
Sacrum
geometric mean
diameter)1/2
Vertical acetabular
Innominate
diameter
bone
Head vertical diameter
Femur
Subtrochanteric
= (subtrochanteric anteroposterior diameter
geometric mean
× subtrochanteric mediolateral diameter)1/2
Midshaft geometric mean = (midshaft anteroposterior diameter ×
midshaft mediolateral diameter)1/2
Geometric mean
= (maximum thickness × maximum height
Patella
x maximum breadth)1/3
Midshaft perimeter
Tibia
Trochlear geometric
= (trochlear length × trochlear breadth)1/2
Talus
mean
Geometric mean
= (maximum length × body length ×
Calcaneus
breadth across the sustentaculum tali ×
height of the body)1/4.
Definition of the variables from Martin and Saller (3) and Bräuer (10) except for the
following: vertical diameter of the humeral head (11), ulnar olecranon height, ulnar
coronoid height, ulnar trochlear anterior-posterior diameter (12) and vertical acetabular
diameter (13).
Table S6. Descriptive statistics and composition of the SH samples used in the
analysis
Sima de los Huesos
Anatomical
Variables
Current Previous
Region
Mean
SD
n
n
15
3
1232.4 96.6
Cranium
Mandibular corpus at
Mandible
12
23.6
2.3
ment. for. GM
Glenoid fossa GM
7
5
29.3
2.0
Scapula
Proximal epiphysis GM
4
4
44.2
3.7
Humerus
Midshaft perimeter
10
9
66.6
8.7
size variation
CV
MR
7.83
1.36
9.97
1.40
6.97
13.07
1.24
1.16
1.51
8
4
59.8
4.6
7.71
1.28
Proximal perimeter
Midshaft perimeter
Neck perimeter
Distal breadth
diameter
diameter
L5 Vertebral body GM
9
12
13
10
13
8
7
8
7
5
-
24.0
44.2
51.1
20.5
38.9
33.1
2.1
4.4
5.1
1.4
3.6
3.5
8.70
9.88
10.03
6.86
9.27
10.51
1.30
1.51
1.43
1.25
1.34
1.32
3
-
49.6
2.0
-
1.08
3
-
49.9
1.6
-
1.06
4
-
40.0
3.1
-
1.19
Sacrum
Lumbosacral surface GM
5
2
40.6
2.7
6.69
1.20
Innominate
bone
Femur
Vertical acetabular
diameter
Subtrochanteric GM
Midshaft GM
GM
Midshaft perimeter
Trochlear GM
GM
7
5
56.7
3.6
6.28
1.20
5
10
7
9
7
15
11
4
8
5
6
8
7
45.2
31.7
29.6
36.5
89.4
30.9
52.8
4.9
2.2
3.8
2.2
8.0
2.4
2.9
10.95
6.81
12.80
6.07
8.97
7.75
5.50
1.27
1.19
1.39
1.21
1.29
1.26
1.18
Ulna
Radius
Vertebrae
Patella
Tibia
Talus
Calcaneus
CV = coefficient of variation; GM = geometric mean; MR = maximum ratio.
Maximum ratio (MR) is equal to maximum value divided by minimum value.
We have not calculated the CV for samples lower than n=5. The previous n is the
number of elements included by Arsuaga et al. (14) and Lorenzo et al. (15). The current
n is the size of the sample used in this analysis.
The following variables were not used by Arsuaga et al. (14) and Lorenzo et al. (15) and
they have been included in this analysis: mandibular corpus at mental foramen
geometric mean, radius proximal epiphysis geometric mean, atlas superior transverse
diameter, axis superior transverse diameter, L5 vertebral body geometric mean and
femur midshaft geometric mean.
Specimens of the Sima de los Huesos sample for:
Cranium: Crania 2-17. Mandibles: AT-1, AT-250+AT-793, AT-300+AT-4147, AT303+AT-1957, AT-505+AT-604, AT-605, AT-792 AT-888, AT-950, AT-1775, AT-2193,
and AT-6726. Scapula: AT-316+AT-1671, AT-320+AT-1750, AT-342, AT-343, AT-794,
AT-2969 and Scapula I. Humerus: AT-93, AT-217, AT-1103, AT-2951+AT-2952,
Humerus II, Humerus III, Humerus VI, Humerus VII, Humerus VIII, Humerus X,
Humerus XI, Humerus XIII, Humerus XIV and Humerus XV. Ulna: AT-488, AT-1104,
AT-1270, Ulna I, Ulna II, Ulna V, Ulna VI, Ulna VII, Ulna VIII, Ulna IX, Ulna X, Ulna
XII, Ulna XIII and Ulna XIV. Radius: Radius I, Radius II, Radius III, Radius IV, Radius
V, Radius VI, Radius VII, Radius IX, Radius X, Radius XI, Radius XIII, AT-349 and
AT-1702. Atlas: VC3, VC7 and VC16. Axis = VC2, VC4 and VC8. Lumbar 5: VL5,
AT-2191, VL12 and VL13. Sacrum: AT-322, AT-1003 (Pelvis 1), AT-1005, AT1234+AT-2721 (Pelvis 2) and AT-3711+AT-4200+AT-4350. Innominate bone: AT-1000
& AT-1001 (Pelvis 1), Coxal I, Coxal II (Pelvis 2), Coxal III, Coxal IV, Coxal V and
Coxal VI. Femur: AT-616, AT-1020, AT-2067, Femur IV+V/2, Femur X, Femur XI,
Femur XII, Femur XIII, Femur XIV+AT-1530, Femur XV and Femur XVI. Patella: AT670, AT-1043, AT-1044, AT-1331, AT-1783, AT-2166, AT-2948, AT-3081 and AT-3297.
Tibia: AT-19, AT-848, AT-2173, Tibia I, Tibia III, Tibia VI and Tibia XII. Talus: AT-860,
AT-965, AT-966+AT-980, AT-1322, AT-1477, AT-1480, AT-1716, AT-1822, AT-1930, AT1931, AT-2495, AT-2803, AT-3132, AT-3133 and AT-4425. Calcaneus: AT-489, AT-663,
AT-969, AT-971+AT-981, AT-1576, AT-1740, AT-2466, AT-3130, AT-3131, AT-3771 and
AT-4426.
Table S7. Percentage of samples generated randomly (n = 5,000) that fall above the SH coefficient of
variation (CV) and SH maximum ratio (MR).
Hamann-Todd Hamann-Todd
Coimbra
Palencia
Euroamericans Afroamericans
Anatomical
Variables
%
%
%
%
%
%
%
%
Region
CV MR CV MR CV
MR
CV
MR
98.7
92.3
83.4
68.3
Cranium
Mandibular corpus at ment.
Mandible
21.6 24.9
for. GM
Glenoid fossa GM
81.2 69.3
Scapula
65.8
Humerus
Midshaft perimeter
8.2
6.1
63.6 43.4
56.5 46.6 53.3
49.5
56.4
33.0
Ulna
Proximal perimeter
86.4 55.6 69.0
52.1
71.0
33.0
Midshaft perimeter
87.9 59.0 61.5
49.7
79.5
65.6
Proximal
epiphysis
GM
89.5
80.7
Radius
Neck perimeter
76.7 79.8
Distal breadth
26.5 39.7
Vertebrae
65.0
diameter
76.2
diameter
L5 Vertebral body GM
43.3
Lumbosacral surface GM
77.3 68.4
Sacrum
Innominate
63.7 56.8
Vertical acetabular diameter
bone
8.4 17.9
18.7
30.3
43.1
27.5
Femur
Subtrochanteric GM
71.2 89.5
90.9
97.4
Midshaft GM
8.9 15.1
23.1
28.6
GM
85.5
82.5
83.6
81.2
Patella
Midshaft perimeter
65.8 57.8 22.1
12.2
54.1
51.1
Tibia
Trochlear GM
43.4 62.1 43.4
71.8
43.4
71.8
Talus
GM
75.5 73.3
49.3
47.4
24.6
25.0
Calcaneus
CV = coefficient of variation; GM = geometric mean; MR = maximum ratio.
Modern human comparative samples from: Coimbra: individuals born in the Beira
Litoral region of Portugal between 1820 and 1920, housed in the Museum of
Anthropology from the University of Coimbra, Portugal. Palencia: individuals deceased
during the last quarter of the XXth century housed in the Anatomical Museum of the
University of Valladolid, Spain. Hamann-Todd Euroamericans and Hamann-Todd
Afroamericans: Cleveland Museum of Natural History, Ohio, USA.
2.4-ENCEPHALIZATION QUOTIENT (EQ)
Table S8. Cranial capacity (CC), estimated body mass (BM) and calculated
encephalization quotient (EQ) for SH sample, Neandertals and two MH samples.
Sample
CC (cm3)
BM (kg)
EQ
Sima de los Huesos
Cranium 2
Cranium 4
Cranium 5
Cranium 10
Cranium 12
Cranium 13
Cranium 15
Cranium 16
Cranium 17
Mean ± SD
Range
Neandertals
Amud 1
La Chapelle-aux-Saints
1
La Ferrassie 1
Spy 2
Shanidar 5
Tabun C1
Mean ± SD
Range
Modern Humans
Pecos (n=29)
Mean ± SD
Range
Euroamericans
Hamann-Todd (n=58)
Mean ± SD
Range
Pooled sample (n=87)
Mean ± SD
Range
1333.5
1360
1092
1218
1227.5
1436.5
1283.5
1236
1218.5
76.8
76.8
57.6
57.6
57.6
76.8
57.6
57.6
57.6
3.32
3.39
3.23
3.61
3.62
3.58
3.80
3.66
3.61
3.54 ± 0.18
3.23-3.80
1750
73.0
4.49
1626
1681
1553
1550
1271
81.7
87.3
86.0
71.2
64.4
3.91
3.88
3.62
4.04
3.52
3.91 ± 0.35
3.52-4.49
3.90 ± 0.37
3.29-4.70
3.80 ± 0.32
2.89-4.52
3.83 ± 0.34
4.70-2.89
The EQ has been calculated as the ratio of the observed brain size (OBS) to the
expected brain size (EBS).
OBS were calculated from CC following the formula from Martin (16): OBS = (CC *
1.018) - 0.025.
EBS was calculated from the respective BM values following the formula from Martin
(16) for Old World simians: Log10 EBS = 0.60 * Log10 BM (in g) + 2.68.
As in Table S4, BM calculated from femoral head diameter (FHD) following Grine et
al. (7). The statistical parameters of the comparative samples have been calculated from
the individual values of EQ. We performed a Mann-Whitney test to compare SH values
with those of Neandertals and modern human samples.
Sima de los Huesos sample: we have used only adult specimens. CC values from
Arsuaga et al. (17). To calculate the EBS we have used two BM, one for individuals
with CC below 1300 cm3 (57.6 kg) and another for individuals with CC above 1300 cm3
(76.8 kg). The larger BM was calculated as the mean of the respective BM calculated
with the FHD of Femur X, Femur XII and Femur XIII and the smaller BM as the mean
of the respective BM calculated with the FHD of Femur XI and Femur XVI (17).
H. neanderthalensis: we have used the following specimens: Amud 1, La Chapelle-auxSaints 1, La Ferrassie 1, Spy 2, Shanidar 5, Neandertal 1, Tabun C1. The CC values are
from Ruff et al. (6). The FHD as in Table S24, except for Shanidar 5 that is from Ruff et
al. (6).
Modern humans: we have used two modern human samples: Pecos (N=29) and
Hamman-Todd (N=58). CC and FHD of Pecos sample from Ruff et al. (6). CC and FHD
of the Hamman-Todd collection has been taken by us.
3- POSTCRANIAL SKELETAL ANATOMY
3.1- COMPARISON OF TRAITS IN THE GENUS HOMO
Table S9. Selected traits in fossil and extant humans
Anatomical Region
Trait
Lower Pleistocene
Homo
H. antecessor
Vertebral canal
dorsoventral diameter
Sima de los Huesos
Non-SH European
Middle Pleistocene
Asian Middle
Pleistocene
African Middle
Pleistocene
Neandertals
Modern Homo
sapiens
Additional
references
Longer
Longer
Shorter
18, 19
Anterior tubercle
Shows a caudal
projection, 100% (n=1)
Shows a caudal
projection
Shows a caudal
projection
Variable (show a caudal
projection: 48.6%)
18-21
Size of the tubercles for
the insertion of the
transverse ligament
Large, 100% (n=1)
Variable: Large (33.3
%); Small (66.7 %)
Small (83.3 %)
Large (74.4-83.3 %)
18-21
Size of the posterior arch
Robust, 100% (n=1)
Atlas
Axis
C6 and C7 spinous
process
Morphology
Robust
Slender
Robust
18, 19
Relatively low and
wide
Relatively low and
wide
Relatively high and
narrow
18, 19
Length
Shorter
Shorter
Longer
Shorter
18, 20
Orientation
More horizontal
More horizontal
Very horizontal
Less horizontal
19, 21
Degree of lordosis of the
lumbar spine
Normal
Hypolordotic
Hypolordotic
Normal
5, 19, 22
Length of the transverse
process
Long?
Long
Long
Short
5, 19
Transverse process
orientation in cranial view
(L2-L3)
Dorso-lateral
Dorso-lateral
Lateral
Dorso-lateral
5, 19, 23
Vertebral canal shape (L4L5)
Normal
Normal
Dorsoventrally enlarged
Normal
5, 19
Lumbar vertebrae
Thorax
Clavicle
Scapula
Humerus
Larger?
Larger
Smaller
19
Relative Length
Longer
Longer??
Longer??
Longer
Shorter
24
Robusticity
Gracile
Gracile
Gracile
Gracile
More robust
11, 25
Frontal curvature or
deflection
Type II
Type II
Type II #
Type II
Variable
11, 21, 26
General size
Glenoid cavity shape
Relatively tall and
narrow
Relatively tall and
narrow #
Relatively tall and
narrow
Relatively low and wide
11, 24
Position of the axillary
sulcus
Dorsal (50%); Ventral
(50%)
High frequency of
dorsal (88.9%)
High frequency of
dorsal (72%)
High frequency of
ventral (90%)
11, 24
Shape of the humeral head
Transversely oval #
Transversely oval
Vertically oval
11
Lesser tubercle
Projecting and
massive
Projecting and massive
Narrow and flat
11
Deltoid tuberosity
Narrow with two
crests #
Olecranon fossa relative
size
Narrower and
shallower
Wider and deeper
Wider and deeper #
Medial pillar relative
thickness
Thicker 100% (n=2)
Thinner 100% (n=2)
Thinner #
Capitulum shape
Taller than wide
Taller than wide ?
Variable: wider than
tall (66%)
Condylo-trochear sulcus
depth
Deep
Deep
Shallow (66%)
Long 100% (n=1)
Absolute and relative neck
length
Radius
Ulna
Narrow with two crests Wide with three crests
11
Wider and deeper
Narrower and shallower
11, 24, 27
Thinner
Thicker
11, 24, 27
Wider than tall
Taller than wide
25
Shallow
Deep
25
Long (75%)
Long
Short
21, 24
Thinner 100% (n=1)
Deep (n=1)
Radial tuberosity position
Medial
Anterior (n=1)
Medial (75%)
Medial (75%)
Anterior
21, 24, 28
Degree of shaft curvature
Low (n=1)
Low (n=1)
High (75%)
High
Low
21
Olecranon size
Larger
Larger
Smaller
29, 30
Trochlear notch
orientation
More anteriorly #
More anteriorly
Antero-proximally
29, 30
Radial notch
Vertically longer #
Vertically longer
Horizontally longer
29, 30
Supinator crest
Short and blunt #
Short and blunt
Long and sharp
Pronator teres crest
Pronounced
Pronounced
Normal
Interosseous crest shape
Short and Blunt #
Short and Blunt
Long and Sharp
Midshaft shape
Rounded #
Rounded
Triangular
Anatomical Region
Trapezium
Trait
Lower Pleistocene
Homo
H. antecessor
Palmar projection of the
tubercle
Concavity of the MC1
facet
Sima de los Huesos
Non-SH European
Middle Pleistocene
Asian Middle
Pleistocene
African Middle
Pleistocene
Neandertals
Modern Homo
sapiens
Less projected
Additional references
Very projected
Very projected
Concave
Relatively flatter
Concave
32
Very projected
Very projected
Less projected
31, 32
31, 32
Hamate
Palmar projection of the
hamulus
Less projected (n=1)
Capitate
Concavity of the MC2
facet*
Concave
Concave
Concave
Concave
31, 32
Pisiform
Shape
Pea-shaped
Pea-shaped
Pea-shaped
32
Lunate
Shape
Relatively short
(proximo-distal)
Relatively long
(proximo-distal)
Relatively long
(proximo-distal)
32
Triquetral
Shape
Relatively broad
(radio-ulnar)
Relatively broad (radioulnar)
Relatively narrow
(radio-ulnar)
32
Metacarpal 1
Size of the attachment for
the opponens pollicis
muscle
Large
Large
Small
32
Morphology
Relatively short with
relatively wide
trochleas
Relatively short with
relatively wide
trochleas
Relatively long with
relatively narrow
trochleas
32
Non-curved
Non-curved
Non-curved
32
Broad
Broad
Narrow
32
Elliptical
Rounded
5, 33-35
Large
Small
4, 5, 34, 36, 37
First proximal hand
phalanx
Proximal hand
phalanges
Curvature*
Distal hand phalanges
Morphology of the distal
tuberosity
Non-curved
Transverse shape
Elliptical
Elliptical
Elliptical
Lateral iliac flaring
Large
Large
Large
Large?
Acetabulocristal buttress
Anteriorly located
Anteriorly located
Anteriorly located
Anteriorly located?
Anteriorly located
Posteriorly located
34, 38, 39
Acetabulospinous buttress
Absent to poorly
defined
Well-defined
Well-defined?
Poorly to well-defined
Absent to well-defined
5, 40, 41
Pelvis
AIIS orientation relative Moderately to strongly
to the anterior iliac margin
twisted
Os coxae
Sacrum
Moderately to
strongly twisted
Strongly twisted
Strongly twisted?
Moderately to strongly
twisted
Non-twisted or only
moderately
38, 40-43
Deep, excavating the
medial surface of the
AIIS
Shallow, not excavating
(or only slightly) to
AIIS
38, 39, 41, 43
Iliopsoas groove
Shallow, not excavating
the medial surface of
the AIIS
AIIS #
AIIS
AIIS?
Supraacetabular sulcus
Conspicuous
Conspicuous
Conspicuous
Conspicuous
Superior pubic ramus
morphology
Thin and plate-like?
Thin and plate-like
Superior pubic ramus
length
Long?
Long
Fusion of the
ventral face of the S1-S2
vertebral bodies
Incomplete
Incomplete
Relative neck length
Longer
Hypotrochanteric fossa
and crest
Constantly present
Conspicuous
Absent or shallow
4, 5, 38, 40, 44, 45
Thin and plate-like
Extremely thin and
plate-like
Thick and bar-like
4, 5, 46, 47
Long
Long
Short
4, 47-49
Variable
Variable (age dependent)
5, 50, 51
Longer #
Constantly present
Large?
Constantly present #
Constantly present
Constantly present
Absent
Absent
Conspicuous
Longer (n=1)
Longer
Shorter
Constantly present
Constantly present
Variable
21, 24, 29
24, 29
Femur
Patella
Tibia
Neck-shaft angle
Low??
Low #
Pilaster
Absent
Absent #
High index > 100%
(taller than wide)
Height/breadth index
Low
High
Absent
Absent
Present
24
Low index < 100%
(wider than tall)
Variable index (80113%)
21, 52
High
Low
52
Low index < 100%
(wider than tall)
Retroversion angle
High #
High
Tibial condyles
displacement
More posterior
position #
More posterior
position
Cross-sectional shape
Amygdaloid
Malleolar facet shape
Talus
Low (n=1)
Head shape
Absolutely and
relatively narrow
Trochlear shape
Rectangular
Rectangular (n=1)
More posterior position More anterior position
Amygdaloid
52
Variable
Very broad
Broad
Narrow
53, 54
Absolutely and
relatively narrow
Absolutely and
relatively broad
Intermediate
53, 55
Rectangular and broad
Wedged-shaped and
narrow
53, 55, 56
Rectangular and broad
Rectangular
General shape
Broad
Broad
Narrow
29, 57
Sustentaculum tali
Well projected
Projected
Less projected
29, 57, 58
Broad
Broad
Narrow
56
Broad
Broad
Narrow
Calcaneus
Fourth metatarsal
Breadth of the base
Distal phalanx Big toe Morphology of the distal
(DP1)
tuberosity
Narrow
Plesiomorphic (blue) and derived (red) trait for the H. neanderthalensis and H. sapiens
clades, except (*) primitive within genus Homo but derived compared to
Australopithecus. Colorless cells indicate uncertain polarity.
AIIS = Anterior Inferior Iliac Spine
#This trait is present in the SH immature individuals
3.2- THORAX AND SPINE
Recent studies have demonstrated that there are significant differences between Homo
neanderthalensis and Homo sapiens in both the vertebral column and ribs (5, 18, 20, 22,
23, 59-61). This is in stark contrast with previous studies that proposed that Neandertals
showed a rather similar configuration in these anatomical regions to modern humans
(29, 62). The SH sample will help elucidate the evolutionary paths that these two
lineages have followed.
Neandertals show differences in both the size and shape of their costal skeleton when
compared to modern humans. Neandertals show longer ribs in the mid-thorax while the
upper-most and lower-most ribs are similar in size to those of Homo sapiens (59). Thus,
the Neandertal thorax is likely larger in size and different in shape than that of Homo
sapiens. There has been some discussion on the exact shape of the Neandertal thorax.
However, quantification of the morphology of the Neandertal thorax has still not been
possible due to the incompleteness of most of the individuals (Shanidar 3, La Chapelleaux-Saints 1, La Ferrassie 1), the presence of taphonomical distortion (Kebara 2, Tabun
C1), pathological lesions (Kebara 2) or errors in the reconstruction (La Ferrassie 1,
Kebara 2) (59). Researchers have suggested different shapes for the thoraces in
Neandertal individuals: more anteroposteriorly enlarged in Shanidar 3 (60) or more
medio-laterally expanded in the case of Tabun C1 (61).
The SH rib collection represents 118 ribs: 58 subadults, 58 adults and 2 of unknown
age-at-death (Table S1). The minimum number of elements (MNE) for ribs 3-10 is
based on the posterior angle. The minimum number of individuals represented is seven,
based on the first rib: three adults, three subadults and one of unknown age-at-death.
The ribs have been separated into two broad categories based on the age-at-death:
subadults and adults. The subadult group includes all the ribs that do not show fusion of
the secondary centers of ossification. In cases in which the head and/or the tubercle are
not present, the porosity of the shaft has been used to tentatively assign an age-at-death:
adults do not show porosity while subadults show porosity.
The SH collection preserves three complete ribs (a 1st, an 11th, and a 12th). However, the
absence of complete mid-thoracic ribs makes it difficult to assess the size and shape of
the SH thorax. Our current working hypothesis is that the SH hominins, like
Neandertals, may have had a larger thorax relative to their stature when compared to
modern humans based on two facts. The first rib SH-Co1 (AT-AT-2748+AT-3546+AT3549) displays a dorsoventral size which is significantly longer than MH and above the
Neandertal sample (four first ribs belonging to two individuals: Kebara 2 and
Regourdou 1) (Table S10). In addition, the comparison of the incomplete costal
fragment AT-2987+AT-3083 with the second rib of Kebara 2 suggests that it was also
longer than the latter. Future discoveries of complete mid-thoracic ribs in SH will make
it possible to test this hypothesis (Figure S3). Additionally, the presence of large
thoraces in the SH hominins would be consistent with the larger anteroposterior and
mediolateral dimensions of the SH articulated pelves (5, 35) (see below). Finally, larger
thoraces would be also expected in these large-bodied (i.e. heavy) hominins (63).
We have proposed elsewhere (5) that most SH individuals likely had 7 cervicals, 12
thoracic, 5 lumbar, 5 sacral and at least 3 coccygeal vertebrae (i.e. 7/12/5/5/>3 vertebral
formula). This is the modal formula in H. sapiens and is also seen in the only complete
adult Neandertal vertebral column found to date (Kebara 2). Based on this evidence, the
last common ancestor of Neandertals and modern humans likely shared this same
vertebral formula. The present analysis of the vertebral morphology is limited to the
cervical and lumbar regions in which the Neandertal and modern human morphologies
are well known (Table S9).
The SH vertebral collection represents 212 vertebrae (Table S1). The minimum number
of elements (MNE) has been calculated in the C1 using the left articular mass and in the
C2 using the odontoid process. In the case of the lower cervicals (C3-C7) we used the
right articular pillar, and in the case of the thoracic and lumbars the vertebral body has
been used. The assessment of the age-at-death is based on the presence/absence of
fusion of the annular epiphyses of the vertebral body and the porosity of the articular
facets (porous in subadults and non-porous in adults).
Regarding the spinal curvatures, the SH hominins, like Neandertals, display a reduced
lumbar lordosis, which is derived in these two hominin groups (5, 22). This assessment
is based on the study of the pelvic incidence (which is correlated with the degree of
lumbar lordosis) in two SH individuals and with a preliminary analysis of the vertebral
wedging in lumbar vertebrae of SH (5, 19).
The SH atlas (C1) displays a large maximum dorsoventral diameter of the vertebral
canal, which is likely related to the large dorsoventral diameter of the foramen magnum.
This feature is also present in Neandertals. Additional features of the atlas include,
among others, a caudally projecting anterior tubercle of the anterior arch and a higher
frequency of small tubercles for the attachment of the transverse ligament than in
modern humans. The frequency of these small tubercles, however, is lower than in
Neandertals. The posterior arch is more robust than in Neandertals and similar in size to
that of modern humans (18, 20). The axis is craniocaudally low and the atlantoaxial
joint is mediolaterally expanded (18). Neandertals are characterized as having long and
horizontal spinous processes in C6 and C7 when compared to modern humans (20). In
fact, both KNM-WT 15000 and Homo antecessor show horizontal spinous processes
(21) although the length is difficult to assess due to their immature status. Thus,
horizontally-oriented spinous processes in the lowermost cervical spine are likely a
plesiomorphic feature. In the case of the C6, the Sima de los Huesos (SH) vertebrae
show a similar spinous process length as modern humans but shorter than those of
Neandertals. The SH specimens show more horizontal angles than modern humans but
not as horizontal as Neandertals. Thus, more vertical angles in modern humans and
longer and even more horizontal spinous processes would be derived in Neandertals
from the possibly plesiomorphic condition displayed by the SH specimens. In the case
of the C7, the SH specimens also show a length of the spinous process that is similar to
modern humans and shorter than Neandertals, but the only specimen which can be
measured shows an angle similar to Neandertals, and below modern humans (Tables
S11-S12, Figure S4). In summary, Neandertals retain a plesiomorphic feature, the
horizontal orientation of the spinous processes, and the longer spinous processes could
be considered as a derived Neandertal feature. At the same time, the less horizontally
oriented spinous processes in modern humans could also be considered as a derived
Homo sapiens feature.
The mid-lower lumbars from SH display long transverse processes in the lumbar
vertebrae based on three different vertebrae (one L3 and two L5) from two different
individuals (5, 19). The comparative analysis of this trait is difficult due to the natural
fragility of this anatomical region, and its scarcity in the fossil record. The Kebara 2
Neandertal appears to show long transverse processes (23). KNM-WT 15000 also
preserves the lumbar transverse processes in several lumbar vertebrae (64), but no
comparative metrical study of this trait has been done. Regarding the orientation of the
transverse process in cranial view, there are significant differences between Neandertals
and modern humans: Neandertals show laterally oriented transverse processes of the
mid-lumbars while in MH they are dorso-laterally oriented (23). The orientation in
KNM-WT 15000 and in SK853 (65) is dorso-lateral which suggests that the orientation
of the transverse process in Neandertals is derived. SH displays the plesiomorphic
orientation as in KNM-WT 15000 and in Homo sapiens (Figure S5). Neandertals also
display a derived dorsoventrally enlarged vertebral canal in L5 which is not present in
the SH hominins nor in H. sapiens (5, 19). In summary, the vertebral column of the SH
hominins shares some derived features with Neandertals but does not display the full
suite of derived Neandertal features.
Table S10. Tuberculo-ventral chord measurements of the 1st rib from SH and
comparisons with Neandertals and a modern human sample
Tuberculo-ventral
chord
Additional
Specimen
Sample/Species
Side
Mean
SD
n
references
Range
SH-Co1
(AT-2748+ATSima de los Huesos
3546+AT-35483549)
Neandertal sample
97.5
L
1
88.9
H. neanderthalensis
-
5.5
L+R
4
67
82.7-94.2
84.7
5.4
R
Euroamerican males
28
74.8-94.5
H. sapiens
L
83.9
4.5
73.9-91.3
67
28
SD = standard deviation; n = sample size. Values in mm.
Definition of “Tuberculo-ventral chord” from (68).
Neandertal sample composed of the first ribs of Kebara 2 and Regourdou 1.
Modern human comparative sample from Gómez-Olivencia et al. (67).
Note that the SH-Co1 rib is above the modern human male and Neandertal sample
ranges.
Table S11. Length and angle of the C6 spinous process in Sima de los Huesos.
Neandertals and modern humans
Maximum
Angle
Additional
Specimen
Sample/Species
length (M13)
(M12)
references
VC12
(AT-3349+AT-3372+AT3373)
VC14
(AT-315+AT-325a+AT325b)
Kebara 2
1
La Ferrassie 1
Shanidar 1
Shanidar 2
Shanidar 3
Sima de los Huesos
29.6
(20)**
Sima de los Huesos
28.3
(30)
(37)
H. neanderthalensis
H. neanderthalensis
33.0
H. neanderthalensis
H. neanderthalensis
H. neanderthalensis
H. neanderthalensis
37.4**
35.0*
28.7
36.4**
26.6 ± 3.5
(18.1-34.7)
n=68
Modern human sample
H. sapiens
[Mean ± SD (Range); n]
(5)**
(19)**
(14)**
38.3 ± 8.8
(26-59.5)
n=19
20
20
20
66
20
20
20
SD = standard deviation; n = sample size. Values in parentheses are estimated.
M13 in mm; M12 in degrees. Definition of the variables from Martin (10).
Values underlined are outside the range of the modern human comparative sample. Zscore values have been calculated on the fossil individuals compared to the modern
human sample. Significantly different values have been indicated as (*=p<0.05;
**=p<0.01).
Table S12. Length and angle of the C7 spinous process in Sima de los Huesos.
Neandertals and modern humans
Maximum
Angle
Additional
Specimen
Sample/Species
length (M13) (M12)
references
VC1
(AT-321 + AT-1556 + Sima de los Huesos
33.3
20
AT-1569 + AT-1609)
AT-2687+ATSima de los Huesos
34.0
3064+AT-4007
AT-3376+AT-3970
Sima de los Huesos
37.8
Kebara 2
36.0
20
H. neanderthalensis
20.5
20
36.5
H. neanderthalensis
15*
1
La Ferrassie 1
20
H. neanderthalensis
41.3**
Regourdou 1
33.2
26
20
H. neanderthalensis
Shanidar 1
(36.0)
29, 66
H. neanderthalensis
Shanidar 2
(34.8)
20
H. neanderthalensis
17*
Shanidar 3
20
H. neanderthalensis
41.8**
34.5 ± 8.5
20
34.1 ± 2.4
(21.0Modern human sample
H. sapiens
(28.0-41.7)
[Mean ± SD (Range); n]
53.0)
n=69
n=27
SD = standard deviation; n = sample size. Values in parentheses are estimated.
M13 in mm; M12 in degrees. Definition of the variables from Martin (10).
Values underlined are outside the range of the modern human comparative sample. Zscore values have been calculated on the fossil individuals compared to the modern
human sample. Significantly different values have been indicated as (*=p<0.05;
**=p<0.01).
Figure S3. Comparison of the incomplete costal fragment AT-2987+AT-3083 (b) with
the right second rib of Kebara 2 (mirrored) (a). This alignment, using the muscle
insertion markings, suggests that the SH rib is dorso-ventrally longer.
Figure S4. Bivariate plot between the length of the spinous process (M13) and its angle
(M12) for the sixth (C6) and seventh (C7) cervical vertebrae. SH and Neandertal
samples are from Tables S10-S11. The dark grey area indicates the Neandertal
morphospace for the individuals in which both variables are present. The light grey area
is the extended morphospace including Neandertal specimens that only preserve the
length of the spinous process. For these specimens a range value (vertical lines) of the
spinous process angle has been estimated based on the range of the most complete
individuals. The dashed vertical lines represent SH specimens for which the spinous
process angle has been estimated based on the range of the most complete Neandertal
individuals.
Figure S5. Cranial view of SH VL2 (L3) (a) compared to the L3 of the Neandertal of
Kebara 2 (b) and the L3 of a modern human (c). Note the more lateral orientation of the
transverse process in Kebara 2.
3.3- SHOULDER GIRDLE AND UPPER LIMB BONES
Table S13. Measurements of the SH adult shoulder girdle and upper limb bones
Pooled-sex
Males
Females
Anatomical
Variable
region
Mean SD n Mean SD n Mean SD
Glenoid index
64.3 4.9 10
Scapula
Robusticity index
22.6 0.5 3 22.2
1
22.9
0.4
Clavicle
Humeral head shape 93.0 2.8 5 93.3 3.1 4
92.1
Humerus
Olecranon fossa
47.9 1.7 8 47.4 0.9 7
51.7
index(*)
Pillar index
29.0 3.9 8 29.7 4.0 6
26.9
3.3
Trochlear notch
Ulna
80.7 4.6 10 82.4 5.4 5
81.6
3.6
orientation
Radial fossa shape
82.0 12.0 12 75.4 14.7 4
95.6
11.2
Robusticity index
15.9 1.9 3 17.8
1
13.9
Diaphyseal index at
75.5 4.1 3 71.7
1
79.8
pronator teres
Neck length index
Radius
11.0 0.9 8 11.0 1.0 6
10.8
0.1
(*)
Curvature index
4.1
0.8 8 4.2
0.9 6
3.7
0.8
SD = standard deviation; n = sample size. “Trochlear notch orientation” in degrees.
Definition of the variables from Martin-M (3), Senut-S (69), Trinkaus (29), Carretero et
al.-C (11), Maia Neto-F (70) and McHenry-McH (12) (see Figure S6 for further details).
Scapula: Glenoid index: M13/M12×100; Clavicle: Robusticity index: M6/M1×100
Humerus: Humeral head index: C3/C4×100; Olecranon fossa index C16/C5×100; Pillar
index: C18/C16×100. Ulna: Trochlear notch orientation: McH8/McH9; Radial fossa
shape: S13/S12; Robusticity index: Midshaft circumference(MSC)/M1×100;
Diaphyseal index at pronator teres: (Min/Max diameter)×100. Radius: Neck length
index: F1b/M1×100; Curvature index: M6.1/M6×100.
Sexual diagnosis of SH upper limb bones following Carretero et al. (2).
n
2
1
1
2
2
2
1
1
2
2
Table S14. Measurements of the SH immature shoulder
bones
Juvenile I
Anatomical
Variable
region
Mean
SD
n
Glenoid index
63.9
5.2
7
Scapula
Robusticity index
23.9
0.1
2
Clavicle
Humeral head shape
Humerus
Olecranon fossa index
48.9
1
(*)
Pillar index
32.2
1
Trochlear
notch
Ulna
orientation
Radial fossa shape
72.6
1
Robusticity index
Diaphyseal index at
79.5
1
pronator teres
Neck length index (*)
12.1
1
Radius
Curvature index
3.2
1
girdle and upper limb
Juvenile II
Mean
SD
n
61.5
2.8
3
49.6
2.8
2
23.6
3.3
2
80.1
-
1
81.6
10.6
-
2
79.3
-
1
11.5
4.2
0.01
1.2
2
2
See Table S13 for further details.
Juveniles I: traces of epiphyseal fusion in their extremities. Juveniles II: epiphyses are
fusing or already fused.
(*) “Neck length” in juvenile individuals was measured as the length from proximal
metaphysis to the upper limit of the radial tuberosity. “Olecreanon fossa index” in
juveniles (Fossa breadth/Distal metaphysis medio-lateral diameter)×100.
Table S15. Measurements of the Neandertal sample shoulder girdle and upper limb bones
Pooled-sex
Males
Females
Anatomical
Variable
region
n
Glenoid index
66.1 3.2 15 67.7 2.7 5
67.7
0.1
2
Scapula
Robusticity index
23.6 2.1 5 23.8 2.4 4
23.0
1
Clavicle
Humeral head shape 98.4 4.4 6 99.6 3.8 5
92.7
1
Humerus
Olecranon fossa
29.1 2.3 23 31.2 1.2 8
26.3
3.0
2
index
Pillar index
26.7 5.5 23 25.3 6.5 8
21.1
0.02
2
Trochlear notch
Ulna
82.4 6.9 11 82.4 5.0 8
78.2
13.7
2
orientation
Radial fossa shape
91.6 25.0 16 67.0 15.0 6 110.1 38.1
2
Robusticity index
14.8
1
Diaphyseal index at
70.1 7.1 3 66.3 3.9 2
77.7
1
pronator teres
Neck length index
9.9
0.5 4 9.8
0.3 3
10.5
1
Radius
Curvature index
4.9
1.2 5 5.9
0.6 2
3.7
1.0
2
Neandertal sample for:
Scapula: Amud 1; La Ferrassie 1 and 2; Neandertal 1; Shanidar 1 and 4; Tabun C1.
Clavicle: Kebara 2; Krapina 142, 143, 144, 145, 149, 153, 154, 155 and 156; La
Chapelle-aux-Saints 1; La Ferrassie 1; Neandertal 1; Regourdou 1; Shanidar 1 and 3.
Humerus: Combe-Grenal; Hortus; Kebara 2; La Chapelle-aux-Saints 1; La Ferrassie 1;
Lezetxiki; Krapina 159, 160, 161, 162, 164, 166, 169, 170, 171, 172 and 174; La Quina
H5; Neandertal 1; Regourdou 1; Spy 1 and 3; Tabun C1; Vilafamés 1. Ulna: Amud 1;
Krapina 179, 181, 182, 183, 184 and 185; La Chapelle-aux-Saints 1; La Ferrassie 1 and
2; La Quina H5. Neandertal 1; Regourdou 1; Shanidar 1, 3, 4, 5 and 6; Spy 1 and 2.
Tabun C1. Radius: Amud 1; Kebara 2; La Chapelle-aux-Saints 1; La Ferrassie 1 and 2;
Neandertal 1; Regourdou 1; Shanidar 1, 4, 5, 6, and 8; Spy 1; Tabun C1.
Table S16. Measurements of the modern human sample shoulder girdle and upper limb
bones
Pooled-sex
Males
Females
Anatomical
Variable
region
Mean SD
n Mean SD n Mean SD
n
Glenoid index
71.5 6.2 111 73.1 6.2 79 67.3 4.5
29
Scapula
Robusticity index
25.4 3.1 262 26.6 2.9 132 24.1 2.8
130
Clavicle
Humeral head shape 108.2 4.3 234 108.1 4.4 129 108.3 4.3
105
Humerus
Olecranon fossa
24.2 2.8 261 25.2 2.8 148 22.9 2.3
113
index
Pillar index
44.2 10.1 258 45.8 9.6 147 41.9 10.5
111
Trochlear
notch
Ulna
68.9 7.2 336 69.2 7.3 170 68.6 7.2
165
orientation
Radial fossa shape
66.9 11.0 330 67.6 11.7 169 66.0 10.2
169
Robusticity index
18.0 1.6 310 18.4 1.6 156 17.6 1.6
152
Diaphyseal index at
85.3 7.6 336 84.5 8.5 163 86.3 6.5
173
pronator teres
Neck length index
9.3
0.8 456 9.5
0.8 243 9.1
0.8
213
Radius
Curvature index
3.2
0.7 462 3.2
0.7 248 3.1
0.6
214
Modern human data from the Hamann-Todd collection, University of Burgos collection,
Natural History Museum Lisboa and Instituto de Antropologia de la Universidade de
Coimbra.
Figure S6. Measurements taken in the upper limb bones. a. Right scapula in lateral
view. b. Left clavicle in superior view. c. Humeral head in medial view; distal right
humerus in posterior view. d. Right ulna in anterior view; and proximal right ulna in
lateral view. e. Proximal left radius in medial view; complete right radius in anterior
view. Numbers refer to definition of the variables from Martin and Saller (3) (M), Senut
(69) (S), Carretero et al. (11) (C), Maia Neto (70) (F) and McHenry et al. (12) (McH).
Figure S7. a. Ulna VII showing a blunt and short supinator crest (lower arrow) and
radial facet shape (upper arrow). b. SH (left) trochlear notch orientation following
Martin and Saller (3) in comparison to those of modern humans (right). (HTH)
Hamann-Todd collection.
Figure S8. Two adult specimens (R-VII and R-VI) showing the variation in neck length
and radial tuberosity position. RVII shows a medially-oriented tuberosity and long neck
while R-VI shows the opposite morphology. Dashed lines mark the interosseus crest.
3.4- HAND
Table S17. Measurements of the SH hand bones compared with Neandertals and
modern humans
Modern
SH
Neandertals
Anatomical
humans
Variable
region
n
Maximum
Lunate
12.1 0.91 8 13.8 1.85 45 14.0 1.43
7
length (M1)
Radio-ulnar
13.9 0.88 8 14.4 1.74 45 15.4 1.46
8
breadth (M2)
Triquetral Maximum
9.0 0.75 7 11.5 1.16 45 9.9
0.78
5
length (M1)
Triquetral
16.1 1.55 3 15.4 1.46 45 16.5 1.84
6
breadth (M2)
Trapezium Dorsopalmar
height of the
9.6 0.85 10 11.0 0.95 45 11.4 1.16
9
MC1 facet (M5)
Dorsopalmar
subtense of the
-1.7 0.32 10 -1.8 0.42 45 -0.9 0.58
6
MC1 facet
Tubercle
5.2 0.79 7 3.3 1.01 45 6.1
1.33
6
projection
MC2/MC3 facet
Capitate
59.7 6.07 6 46.0 7.0 41 60.0 10.11 8
angle
Articular length 15.9 0.85 9 18.4 2.01 45 17.5 1.50
7
Hamate
Hamulus
projection (Max.
10.5 0.63 5 9.3 1.63 45 11.0 1.87
8
height - Body
height) (M5)
Articular length 25.9 0.44 8 28.9 2.46 96 27.6 1.31 10
PP1
Proximal
16.8 1.64 9 15.9 1.39 96 16.7 1.41 10
breadth
Articular length 21.6 4.00 11 22.2 2.09 96 24.3 0.94 15
DP1
Distal breadth
12.2 2.40 9 10.1 1.21 96 12.8 0.70 15
PP1 = thumb proximal phalanx; DP1 = thumb distal phalanx.
Variables in mm except “Capitate MC2/MC3 facet angle” in degrees.
Definition of the variables from Martin and Saller (3) and Bräuer (10) except for the
following: dorso-palmar subtense of the MC1 facet and trapezium tubercle projection
(29); capitate MC2/MC3 facet angle (71); hamate articular length (32); phalangeal
articular length, proximal breadth, distal breadth (72).
Modern human data obtained in the Hamann-Todd collection (CMNH).
Neandertal and modern human data for “Capitate MC2/MC3 facet angle” from
Niewoehner et al. (71).
Neandertal sample composed of La Ferrassie 1 and 2, La Chapelle-aux-Saints 1, Kebara
2, Regourdou 1, Shanidar 3, 4 and 7, Tabun C1, Amud 1, Krapina 200, 202. 202.1,
202.2, 203.1, 203.2, 203.3, and 203.4, Kiik-Koba.
3.5- PELVIC GIRDLE
Inventory and sex attribution. The pelvic sample is currently composed of 156 isolated
fragments (os coxae, sacrum and coccyx), representing a minimum number of 49
elements (MNE=49) from at least 17 individuals (MNI=17). Specimens with signs of
incomplete ossification of the os coxae, sacrum and coccygeal vertebrae have been
considered as subadult elements/individuals. The os coxae has been classified as adult
when showing complete fusion of the iliac crest and/or ischial tuberosity epiphyses
(some traces of recent fusion could be still visible). The sacrum is considered adult
when fusion of the sacroiliac epiphysis and union of the sacral bodies are complete (S1S2 joint could show partial obliteration). Coccygeal vertebrae are considered to be adult
when the ossification of the vertebral body and of the cornua and annular rings (first
coccygeal vertebra) is complete. According to these criteria, 10 out of 17 individuals are
osteologically immature, while five of them possessed fully developed pelves. The
remaining two individuals are represented by more fragmentary remains and they were
close to or already had fully mature pelves.
As previously described, the SH pelvic sample shows a certain degree of variation in
modern sex-linked morphological features (4, 5). Those morphological features
consistent with the male-like condition include larger size and robust muscle
attachments, a narrow greater sciatic notch, absence of ventral arc and subpubic
concavity and a broad flat surface of the medial aspect of the ischio-pubic ramus. In
contrast, modern female-like morphology is characterized by smaller size and lower
robusticity, a wider sciatic notch, development of the ventral rampart, presence of a
moderate subpubic concavity, a mediolaterally (M-L) larger pubic body, acute medial
aspect of the lower pubic ramus and a wider subpubic angle. Relying on this pattern of
variation, three adult individuals have been considered to be males (including the almost
complete articulated Pelvis 1, the partially complete Pelvis 2 and Coxal IV) and another
three individuals are likely females [one adult -Coxal III- and two subadult individuals,
one of them (Coxal I) had just reached full ossification of the acetabulum and the other
one (Coxal V) shows a mature acetabulum but non-fused iliac crest epiphysis].
Ontogeny of pelvic traits. The appearance of several of the morphological pelvic
features figured in Table S9 can be traced through development in the SH sample.
Immature individuals [both with unfused and actively fusing epiphyses of the anterior
inferior iliac spine (AIIS) and triradiate cartilage] shows an AIIS orientation and
iliopsoas groove configuration similar to the variation found in their fully adult
counterparts. Another set of features, including the development of the supraacetabular
sulcus and the acetabulospinous and acetabulocristal buttresses and the morphology of
the superior pubis ramus are established at different ontogenetic stages, reaching the
fully adult morphology between the end of adolescence (fusion of iliac and ischial
tuberosities) and the attainment of bony maturity (complete epiphyseal ossification).
SH sample vs MH sample comparison. SH metrical data are compared with a pooledsex MH sample (Table S18). We are aware of the potential for a sex bias in the SH
composition that could be hampering the significance of this comparison. Moreover, SH
mean values for the selected pelvic variables include individuals attributed to males,
females and individuals of indeterminate sex. In most cases the individuals contributing
to the SH mean value for each variable produced unbalanced sex samples. To account
for potential statistical differences influenced by the SH sex composition, we have also
compared differences between male and female modern samples and SH using the
Mann-Whitney U-test.
Compared to modern males, the SH sample is significantly different (p<0.05) in the
maximum coxal height, in the maximum iliac breadth and the nonarticular pubic length
(both at the p<0.017 level) and in the iliac height, the nonarticular ischial length, the
superior pubic ramus height and the maximum sacral breadth (all at the p<0.01 level).
On the other hand, the sacral length, the cotylosciatic breadth and the acetabular vertical
diameter do not reach statistical significance. Compared to females, the SH sample is
significantly different in the sacral length at the p<0.05 level, in the maximum iliac
breadth, the nonarticular pubic length and the cotylosciatic breadth, all at the p<0.017
level, and for the remaining variables figured in Table S18 at the p<0.01 level. The
superior pubic ramus height does not reach statistical significance.
In summary, it is important to point out that: i) the vertical acetabular diameter and the
sacral length in the SH sample are statistically different from both the pooled-sex and
female modern human samples, but not the male sample; ii) the superior pubic ramus
height is different from both the pooled-sex and male modern human samples, but not
the female sample; iii) the cotylosciatic breadth is only different from the female
modern human sample; iv) the remaining variables offer similar results when SH is
compared to male, female and pooled-sex modern samples. Therefore, the results of the
comparisons between SH and modern humans are quite consistent despite the
potentially unbalanced sex ratio of the SH sample.
SH sample vs. Neandertal sample comparison. Significant differences found between
the iliac height of the SH and Neandertal samples could be affected by the fragmentary
preservation of the ilium of several of the Neandertal specimens included in the analysis
(Krapina 207, Neandertal 1 and Amud 1). This state of preservation likely results in a
slight underestimation of the Neandertal mean value (Table S18).
Table S18. Measurements of the SH pelvis compared with Neandertals and moder
humans
SH
Modern humans
Neandertals
Mean SD
Mean
SD
n
Mean
SD
n
Variable
n NMI
Range Range Range 229.1 12.7
4
204.5** 12.3 390 202.0 22.0
Maximum coxal
3
3
height (13)
215.1-240.0 166.0-239.0 178.4-221.5 †
178.6
8.0 357
154.4
Maximum iliac
2
2
breadth (13)
130.0-185.0 176.3-180.8 140.1 2.0
5
121.6** 7.0 384 124.0* 10.4
Iliac height (13)
3
3
138.7-142.4 97.8-143.6 111.3-134.5 53.5 5.1
4.1 398 46.0
6.9
7
46.1**
Nonarticular ischial
8
6
length (73)
45.1-60.9 34.2-56.1 37.2-54.5 †
87.3
4.5 354 86.0
6.0
6
68.1
Nonarticular pubic
2
2
length (13)
83.9-90.7 54.6-81.0 78.7-93.0 10.4 0.3
2.1 73 8.0**
1.3
7
12.6*
Superior pubic
4
3
ramus height (68)
10.0-10.7 8.0-18.0 5.7-9.4 35.7 1.8
35.3
3.5 407 33.0
4.2
12
Cotylosciatic
7
6
breadth (74)
32.6-38.4 26.9-45.5 27.9-39.9 **
56.7 3.6
3.8 399 56.2
6.4
9
52.7
Vertical acetabular
7
7
diameter (13)
50.0-60.0 41.7-62.0 41.0-62.0 †
Maximum sacral
125.0 2.8
7.7
6
113.7** 7.5 75 112.4
breadth (See
5
5
121.1-128.5 93.6-132.9 103.4-122.4 footnote)
117.7
8.5 75 107.7
5.8
3
106.2*
Sacral length,
2
2
straight (75)
116.5-118.9 77.7-130.1 102.0-113.6 SD = standard deviation; n =sample size; MNI= minimum number of SH individuals
represented by each variable. Variables in mm.
SH data is based on specimens showing mature morphology of the region involved in
each variable.
Modern human data (pooled-sex sample) from the Instituto de Antropologia de la
Universidade de Coimbra, except “Superior pubic ramus height” data (pers. comm. Yoel
Rak). Regarding the sacrum, only individuals with five vertebrae have been included in
the analysis.
Neandertal sample composed of Krapina 207 Cx 1, 208 Cx 2, 209+212 Cx 3/6, 255.7,
255.10, La Chapelle-aux-Saints 1, La Ferrassie 1, Neandertal 1, Regourdou 1, Subalyuk
1, Amud 1, Kebara 2, Shanidar 1, Shanidar 3, Tabun C1.
Definition of the variable in parenthesis, except “Maximum sacral breadth: transverse
breadth taken between the most lateral points of the sacral wings”.
A Mann-Whitney’s U-test has been performed between the SH and modern humans and
SH and Neandertal samples. Significantly different values have been respectively
indicated on the modern human and Neandertal means using *=p<0.05; **=p<0.01.
Applying the Dunn-Šidák correction for multiple comparisons [1 - (1 - α)1/n] with an
α=0.05 and three groups(n) threshold value for significance is 0.017 and is indicated
using †.
Figure S9. Morphological traits of the SH innominate bones. Lateral (a), medial (b),
dorsal (c) and ventral (d) views of AT-1000 hip bone (Pelvis 1). Ventral view (e) of AT1006 pubis. Lateral view (f) of AT-3497+AT-3813+AT-3814 pubis. 1-Supraacetabular
sulcus. 2- Sigmoid shape with anteriorly projected anterior superior iliac spine (ASIS)
and AIIS. 3-Distinct acetabulospinous pillar. 4-Large and prominent iliac tuberosity and
well-delimited postauricular sulcus. 5- Marked lateral iliac flaring, strongly developed
acetabulocristal pillar and robust iliac tubercle (relative to H.sapiens). 6-Dorsolaterally
facing ischial tuberosity. 7-Moderately to strongly twisted AIIS. 8-Deep iliopsoas
groove that excavates to the medial surface of the AIIS. 9-Flat to slightly concave
pectineal surface with a thin and prominent crest. 10-Rectangular plate-like morphology
of the superior pubic ramus.
Figure S10. Morphological traits of the SH sacra. Superior (a), ventral (b) and dorsal
(c) views of AT-1005 sacrum. 1-Distinct dorsal alar tubercle. 2-Auricular surface
caudally extended from the S2 caudal edge to mid-S3. 3-Junction between the bodies of
the S1-S2 vertebrae with incomplete fusion and “second promontory” morphology. 4Presence of intermediate dorsal crest. 5-Well-developed sacral tuberosity with at least
two fossae for sacroiliac ligaments. See also Fig. S8 of Bonmatí et al. (5).
3.6-LOWER LIMB BONES
Linea aspera. The linea aspera is frequently elevated by an underlying bony ridge or
pilaster resulting in a prismatic, cross-sectional configuration. A prominent linea aspera
is not always accompanied by a well-developed pilaster (76). According to Trinkaus and
Ruff (77) all of the late archaic humans they studied have cross-sections which are
subcircular to ovoid, with varying degrees of development of the linea aspera, but none
of them exhibits either a concavity adjacent to the linea aspera associated with a pilaster
or a flatness of the bone adjacent to the linea aspera producing a blunt angle across the
posterior margin of the cross-section. Although in the SH sample there are varying
degrees of development of the linea aspera, none of the SH specimens have a clear
pilaster sensu Homo sapiens.
The neck-shaft angle. The neck-shaft angles of SH femora are well within modern
human variation, but the sample is, on average, below many recent human sample
means (for example, only 6% of individuals in our modern sample are below 115 degrees).
Table S19. Measurements of the SH adult lower limb bones
Anatomical
region
Femur
Tibia
Variable
Neck length index
Midshaft index
Trochanteric index
Curvature index
(M31)
Bicondylar angle
(M30)
Neck angle (M29)
Tuberosity
projection/retroversion
tibial fossa
Midshaft index
Proximal shaft index
SH
Pooled-sex
Males
Mean SD n Mean SD
10.5 0.3
92.2 5.8
75.4 8.3 4 81.0
-
n
3
4
2
Females
Mean SD
69.8
-
-
4.1
0.3
3
-
-
78.6
2.1
3
-
n
2
112.8
4.0
5 113.7
4.0
3
111.5
-
2
43.6
3.6
7
45.1
2.6
5
39.9
-
2
70.7
65.9
6.9
5.4
7
6
68.5
65.6
7.0
60.5
5
5
76.1
67.2
-
2
1
SD = standard deviation; n = sample size. “Neck angle” in degrees.
Definition of the variables from Martin and Saller-M (3), McHenry and Corruccini-MC
(78) and Trinkaus and Rhoads (52) (see Figure S11 for further details).
Femur: Neck length index: MC7/MC11×100; Midshaft index: MC15/MC14×100;
Trochanteric index: MC5/MC4×100. Tibia: Midshaft index: M8/M9×100. Proximal
shaft index: M8a/M9a×100.
Sexual diagnosis of SH lower limb bones following Carretero et al. (2).
Table S20. Measurements of the SH immature lower limb bones
SH
Anatomical
Variable
Juvenile I
Juvenile II
region
Mean
SD
n Mean
SD
Neck length index(*)
14.9
1.4
4
Femur
Midshaft index
102.7
4.7
12 100.9
5.3
Trochanteric index
Curvature index (M31)
2.6
0.8
4
2.1
Bicondylar angle (M30)
69.6
4.8
5
75
Neck angle (M29)
121.7
3.1
8
119
6.6
Tuberosity
Tibia
projection/retroversion
tibial fossa
Midshaft index
78.8
1
74.2
1
-
n
3
1
1
3
Juveniles I: traces of epiphyseal fusion in the extremities. Juveniles II: epiphyses are
fusing or already fused. No comparative data is presented for these age groups because
equivalent measurements are not available in the fossil record.
(*) “Neck length” in juvenile individuals was measured as the length from the edge of
the proximal metaphysis in posterior view to the intertrochanteric crest.
Table S21. Measurements of the Neandertal lower limb bones
Neandertals
Anatomical
Variable
Pooled-sex
Males
Females
region
Neck length index
12.0 1.4 6 12.4 1.1 5
9.8
Femur
Midshaft index
99.6 11.1 19 93.7 10.2 9 108.9 12.5
Trochanteric index
79.1 6.7 19 79.9 7.4 13 76.4
4.2
Curvature index
(M31)
Bicondylar angle
83.3 1.5 3
84
2
82
(M30)
Neck angle (M29)
118.6 5.0 8 116.3 3.1 6 125.5
Tuberosity
Tibia
projection/retroversio 44.1 5.9 7 47.4 1.9 5 36.0
n tibial fossa
Midshaft index
69.7 4.1 4 68.2 3.2 3 74.4
73.6 8.4 4 69.4 1.2 3 86.1
Neandertal sample:
Femur: Amud 1, Fond-de-Forêt, La Chapelle-aux-Saints 1, La Ferrassie 1 and 2, La
Quina H5, Neandertal 1, Shanidar 1, 4, 5 and 6, Spy 2, Tabun C1. Tibia: Kiik-Koba 1,
La Chapelle-aux-Saints 1, La Ferrassie 2, Spy 2.
n
1
3
5
1
2
2
1
1
Table S22. Measurements of the modern human lower limb bones
Modern humans
Anatomical
Variable
Pooled-sex
Males
region
Mean SD
n Mean SD n
Neck length index
7.9 1.5 411 7.9 1.4 255
Femur
Midshaft index
95.8 9.2 416 95.9 9.4 258
Trochanteric index
87.3 12.3 416 86.2 7.0 98
Curvature index
2.8 1.0 133 2.7 0.9 85
(M31)
Bicondylar angle
81.4 3.3 108 81.2 3.1 98
(M30)
Neck angle (M29)
125.7 7.0 150 126.0 6.6 91
Tuberosity
Tibia
projection/retroversion 37.8 4.0 187 37.7 3.8 114
tibial fossa
Midshaft index
79.4 8.8 381 78.7 9.1 203
76.4 7.5 386 75.4 7.0 203
Females
Mean SD
n
7.8 1.5 155
95.5 8.7 157
85.8 8.0 158
3.0
1.2
48
80.6
3.1
66
125.2 7.6
59
37.9
3.8
73
80.3
77.4
8.6
8.0
178
183
Modern human data from the Hamann-Todd collection, and University of Burgos
collection as well as the Natural History Museum of Lisboa and the Instituto de
Antropologia de la Universidade de Coimbra.
Figure S11. Graphic representation of femur measurements. Numbers refer to definition
of the variable from Martin and Saller (3) (M) and McHenry and Corruccini (78) (MC).
Figure S12. Adult (TIB-XII, left) and subadult (TIB-II, right) tibia specimens showing
the posterior position of the plateau relative to the diaphyseal anatomical axis, the
retroversion angle and the curvature variation.
3.7- FOOT
Table S23. Measurements of the SH foot bones compared with Neandertals and modern
humans
SH
Modern humans
Neandertals
Anatomical
Variable
Mea
region
Mean SD n Mean SD
n
SD
n
n
Talar length (M1)
51.9 3.5 18 52.8 4.0 162 51.2 3.5 21
Talus
Lateral malleolar
13.2 2.0 20 9.4
2.2 112 10.7 2.5 24
breadth (M7a)
Length of the head
30.4 2.2 18 32.5 2.9 161 34.7 3.4 23
(M9)
Trochlear height
9.1
1.0 18 8.4
1.0 162 9.5 1.3 22
(M6)
Calcaneus breadth
Calcaneus
44.6 3.0 14 40.0 3.7 164 44.2 3.6 14
(M2)
Breadth of
17.6 2.4 14 14.2 2.6 114 15..3 3.6 14
sustentaculum tali
(M6)
Total length (M2)
78.7 2.9 4 73.3 4.8 153 72.5 5.5 14
Second
metatarsal
Proximal articular
13.3 0.5 5 13.3 1.2 153 15.0 2.0 13
breadth (M6b)
Total length (M2)
70.3
2 70.3 4.9 147 67.9 6.0 14
Fourth
metatarsal
Proximal breadth
14.8 0.4 4 13.2 1.3 151 15.3 1.0 12
(M6a)
Maximum length
Proximal
34.0 1.4 7 35.0 2.9 244 27.6 3.9 23
(M1)
Phalanx I
Breadth of diaphysis
14.0 1.6 8 12.1 1.6 244 13.1 1.7 22
(M2)
Distal Phalanx I Breadth of the distal
14.6 2.1 8 11.8 1.6 169 14.9 2.7 10
tuberosity (M2b)
Variables in mm. Data from Pablos et al. (53, 56, 57) and present study. Definition of
the variable from Martin and Saller-M (3) and Bräuer (10). Modern human data from
the Hamann-Todd collection. Neandertal sample: Talus: Amud 1, Kiik-Koba 1 (right
and left), Krapina 235, 236, 237, 238.1, 238.2+238.7, 238.4, 239.1, 239.2, La Chapelleaux-Saints 1, La Ferrassie 1 and 2 (right and left), La Quina H1 (right and left),
Regourdou 1 (right and left), Shanidar 1 and 3 (right and left), Spy 2, Tabun C1 (right
and left). Calcaneus: Amud 1, Kiik-Koba 1 (right and left), Krapina 240, La Chapelleaux-Saints 1, La Ferrassie 1 and 2 (right and left), Regourdou 1 and 2, Shanidar 1 (right
and left), Shanidar 3, Spy 2, Tabun C1. Metatarsal II: Amud 1 (right and left), KiikKoba 1 (right and left), La Ferrassie 1 and 2 (right and left), Sedia del Diavolo 2,
Shanidar 1, 3 and 6 (right and left), Shanidar 4 left, Sima de las Palomas 92, Spy 2,
Subalyuk 1, Tabun C1 (right and left). Metatarsal IV: Kebara 9, Krapina 248.1, 248.2,
248.3, La Chapelle-aux-Saints 1, La Ferrassie 1 (left) and 2 (right and left), Regourdou
1, Shanidar 1 (right), 6 (right) and 8 (right and left), Sima de las Palomas 92, Subalyuk
1 (right and left), Tabun C1. Proximal Phalanx I: Combe Grenal 845, Kebara 10, KiikKoba I (right and left), Krapina 252.2, 252.3, 252.4, La Ferrassie 2, Shanidar 1, 4, 6 and
8, Regourdou 1 (right and left).
4- EVOLUTION OF THE BODY IN THE GENUS HOMO
Table S24. Material and data for the analysis of the evolution of the body in the
genus Homo
Sample
Specimen
FML ACH FHD BIB
Reference
KNM-ER 3228
55.5 46.3#
35, this study
Early
KNM-ER 1472
401
79
Pleistocene
KNM-ER 1481
396
44.0
79
Homo 1
KNM-ER 3728
390
79
(2.0-1.8 Myrs)
Dmanisi 4167
386
40.0
80
KNM-ER 737
420
79
KNM-ER 1808
480
79
79, S. Simpson
KNM-WT 15000
255.0- and S.
432
(Immature)
266.0
Spurlock, pers.
Early
com.
Pleistocene
Homo 2
KNM-WT 15000
S. Simpson and
(1.7-0.8 Myrs) (Adult
300.0 S. Spurlock,
estimation)
pers. com.
BSN49/P27
41.0 32.6#
288.0
34
375OH 34
395
81
OH 28
450
47.6
79, this study
KNM-ER 999
482
82, 83
Zhouk Fem 1
400
44
Zhouk Fem 4
407
44
Non-SH
Berg Aukas
56.4
7
middle
Arago 44
60.6 51.2#
This study
Pleistocene
Broken Hill 689
49.5
6
Homo
Broken Hill 719
60.1 50.7#
This study
Broken Hill 907
52.5
6
Jinniushan 1
60.0 50.6#
344.0 33
Le prince 1
59.0 49.7#
39
Femur IV
46.5
84
Femur V
46.5
84
Femur X
458
52.8
2, this study
Femur XI
41.8
This study
Sima de los
Femur XII
450
49.0
2, this study
Huesos
Femur XIII
450
48.3
2, this study
Femur XVI
41.2
This study
Pelvis 1
335.0
5
Pelvis 2
338.4
This study
Amud 1 (L)
484
57.1 47.9#
38, this study
Kebara 2 (R)
59
48.0#
313.0
6, this study
La Chapelle-aux292.0
Saints 1 (R)
430
52.1
6, 85,86
Neandertals
La Ferrassie 1
(R)
56.0
44
La Ferrassie 1
465
44
(L)
Neandertal 1 (L)
Shanidar 1 (R)
Spy 2 (R)
La Ferrassie 2
(L)
Tabun C1 (R)
Modern
Humans
Sima de las
Palomas 96 (R)
Krapina 207
Krapina 208
Krapina 209
Krapina 213
Krapina 214
Mean
SD
Max
Min
n
444
461
425
52.0
411
46.0
416
40.0
53.0
391.5
54.3
55.5
54.9
434.6
28.2
488
380.6
67
44
29
44
43.0
45.2#
46.3#
45.8#
52.7
44.2
45.0
4.0
54.56
38.27
67
260.0
44
44, 68, This
study
87
This study
This study
This study
6
6
262.0
15.5
306.0
220.0
255
FML = femoral maximum length; ACH = acetabular height; FHD = femoral head
diameter; BIB = Bi-iliac breadth
#FHD calculated from vertical acetabular diameter following Ruff (36).
Modern human sample comes from Hamann-Todd and University of Iowa (Femoral
maximum length and head diameter) and Coimbra (Bi-iliac breadth). See also Table
S25.
5- MATERIALS EXAMINED IN THIS STUDY
Table S25. Comparative material used in this study
Specimen/sample
Source
Additional references Modern humans Hamann-Todd Osteological
O
collection: Euroamericans
Hamann-Todd Osteological
O
collection: Afroamericans
University of Burgos:
O
Osteological collection:
Europeans
University of Iowa
O
Osteological collection:
Euroamericans
Instituto de Antropologia
O
de la Universidade de
Coimbra: Europeans
Natural History Museum
O
Lisboa: Europeans
6
Pecos
B
Neandertals Amud 1
O. C. B
6, 38, 88
Combe Grenal 845
B
89
Dederiyeh 8906
B
90
Kebara 2 and 9
O. C. B
6, 50, 59, 91-93
Kiik-Koba 1
C
88, 94
Krapina sample
O. C. B
6, 88, 95-98
La Chapelle-aux-Saints 1
O
6, 20, 85, 86, 99
La Ferrassie 1 and 2
O. C
20, 44, 100, 101
La Quina H1 and H5
C. B
88, 102
Le Moustier 1
C
17
Moros de Gabasa
O. B
103
Neanderthal 1
O. C. B
6, 44
Regourdou 1 and 2
O. B
20, 42, 104-106
Sedia del Diavolo 2
B
107
Shanidar 1, 2, 3, 4, 5, 6 and
O. C. B
6, 29, 60, 66, 88, 95, 108-110 8
Sima de las Palomas 92
B
87, 111 and 96
Spy 2 and isolated
C. B
6, 44, 88, 112 elements
Subalyuk 1
B. C
113
Tabun C1
O. B
6, 44, 61, 68, 114, 115 Early Modern Humans Qafzeh 7, 8, 9
B
Skhul IV, V, VII
B
European early Pleistocene Homo
Homo antecessor-TD6
O
European middle Pleistocene Homo
Arago 44
C. B
Grotte du Prince
B
Vilafamés 1 and 2
O. C. B
Asian middle Pleistocene Homo
Jinniushan
B
Zhoukoudian
B
African middle Pleistocene Homo
Berg Aukas
B
Broken Hill (E-691. E.719.
O. B
E-898 )
OH 28
C. B
African and Asian early Pleistocene Homo
BSN49/P27
B
D4167
B
KNM-ER 737
B
KNM-ER 813A
C
KNM-ER 1464
C
KNM-ER 999
B
KNM-ER 1472
B
KNM-ER 1476a
C
KNM-ER 1481
B
KNM-ER 1808
B
KNM-ER 3228
C. B
KNM-WT 15000
C. B
OH 34
SK-853
B
B
O = original; C = cast; B=bibliography 105
68
21, 27, 31, 56, 67
40, 116
39
117
33, 55, 118
44
7
6, 25, 45, 119 116, 120
34
80
79
121
121
82, 83
79
121
79
79
35, 43
36, 122, S. Simpson and S. Spurlock,
pers. com.
78
64
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Postcranial morphology of the middle Pleistocene humans from

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