The Later Stone Age Calvaria from Iwo Eleru, Nigeria: Morphology and Chronology

Abstract

In recent years the Later Stone Age has been redated to a much deeper time depth than previously thought. At the same time, human remains from this time period are scarce in Africa, and even rarer in West Africa. The Iwo Eleru burial is one of the few human skeletal remains associated with Later Stone Age artifacts in that region with a proposed Pleistocene date. We undertook a morphometric reanalysis of this cranium in order to better assess its affinities. We also conducted Uranium-series dating to re-evaluate its chronology.
A 3-D geometric morphometric analysis of cranial landmarks and semilandmarks was conducted using a large comparative fossil and modern human sample. The measurements were collected in the form of three dimensional coordinates and processed using Generalized Procrustes Analysis. Principal components, canonical variates, Mahalanobis D(2) and Procrustes distance analyses were performed. The results were further visualized by comparing specimen and mean configurations. Results point to a morphological similarity with late archaic African specimens dating to the Late Pleistocene. A long bone cortical fragment was made available for U-series analysis in order to re-date the specimen. The results (∼11.7-16.3 ka) support a terminal Pleistocene chronology for the Iwo Eleru burial as was also suggested by the original radiocarbon dating results and by stratigraphic evidence.
Our findings are in accordance with suggestions of deep population substructure in Africa and a complex evolutionary process for the origin of modern humans. They further highlight the dearth of hominin finds from West Africa, and underscore our real lack of knowledge of human evolution in that region.

Full text

The Later Stone Age Calvaria from Iwo Eleru, Nigeria:
Morphology and Chronology
Katerina Harvati
1
*, Chris Stringer
2
, Rainer Gru
¨
n
3
, Maxime Aubert
3
, Philip Allsworth-Jones
4
, Caleb
Adebayo Folorunso
5
1 Paleoanthropology, Senckenberg Center for Human Evolution and Paleoecology, Eberhard Karls Universita
¨
tTu
¨
bingen, Tu
¨
bingen, Germany, 2 Paleontology Department,
Natural History Museum, London, United Kingdom, 3 Research School of Earth Sciences, The Australian National University, Canberra, Australia, 4 Department of
Archaeology, University of Sheffield, Sheffield, United Kingdom, 5 Department of Archaeology and Anthropology, University of Ibadan, Ibadan, Nigeria
Abstract
Background:
In recent years the Later Stone Age has been redated to a much deeper time depth than previously thought.
At the same time, human remains from this time period are scarce in Africa, and even rarer in West Africa. The Iwo Eleru
burial is one of the few human skeletal remains associated with Later Stone Age artifacts in that region with a proposed
Pleistocene date. We undertook a morphometric reanalysis of this cranium in order to better assess its affinities. We also
conducted Uranium-series dating to re-evaluate its chronology.
Methodology/Principal Findings:
A 3-D geometric morphometric analysis of cranial landmarks and semilandmarks was
conducted using a large comparative fossil and modern human sample. The measurements were collected in the form of
three dimensional coordinates and processed using Generalized Procrustes Analysis. Principal components, canonical
variates, Mahalanobis D
2
and Procrustes distance analyses were performed. The results were further visualized by
comparing specimen and mean configurations. Results point to a morphological similarity with late archaic African
specimens dating to the Late Pleistocene. A long bone cortical fragment was made available for U-series analysis in order to
re-date the specimen. The results (~11.7–16.3 ka) support a terminal Pleistocene chronology for the Iwo Eleru burial as was
also suggested by the original radiocarbon dating results and by stratigraphic evidence.
Conclusions/Significance:
Our findings are in accordance with suggestions of deep population substructure in Africa and a
complex evolutionary process for the origin of modern humans. They further highlight the dearth of hominin finds from
West Africa, and underscore our real lack of knowledge of human evolution in that region.
Citation: Harvati K, Stringer C, Gru
¨
n R, Aubert M, Allsworth-Jones P, et al. (2011) The Later Stone Age Calvaria from Iwo Eleru, Nigeria: Morphology and
Chronology. PLoS ONE 6(9): e24024. doi:10.1371/journal.pone.0024024
Editor: John H. Relethford, State University of New York College at Oneonta, United States of America
Received May 17, 2011; Accepted August 4, 2011; Published September 15, 2011
Copyright: ß 2011 Harvati et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The work was funded by Senckenberg Research Institution, University of Tu
¨
bingen. The funders had no role in study design, data collection and
analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: katerina.harvati@ifu.uni-tuebingen.de
Introduction
The Iwo Eleru burial was excavated from the Iwo Eleru rock
shelter, south-western Nigeria, in 1965 by Thurstan Shaw and his
team (Figure 1). The skeleton, preserving a calvaria, mandible and
some postcranial remains, was found at a depth between 82 and
100 cm from the surface in an undisturbed Later Stone Age
(hereafter LSA) context. Radiocarbon analysis of charcoal from the
immediate vicinity of the burial resulted in an age estimate of
11,2006200 BP (,13 ka calibrated). The skull was reconstructed
and studied by Brothwell [1] (Figure 1)], who linked it to recent
West African populations, though he recognized that its lower vault
and frontal profile were unusual, and that the mandible was robust.
The specimen is complete along the entire midline from nasion to
beyond opisthocranion. Although it slightly asymmetric it shows no
major distortions and the relatively well preserved mandible
constrains its basal breadth. A preliminary multivariate analysis of
cranial measurements by Peter Andrews (in [1]) suggested that the
Iwo Eleru specimen was distinct from recent African groups.
A more extensive analysis of the cranial measurements of the
original Iwo Eleru specimen was conducted by Chris Stringer,
who included this cranium in univariate and multivariate
(Canonical Variates, Generalised Distance) analyses for his
doctoral thesis [2,3]. Coefficients of separate determination in a
cranial analysis using 17 of Howells’ measures showed that the
main discriminators from an Upper Paleolithic sample were low
frontal subtense, low vertex radius, high cranial breadth, high
bifrontal breadth, high cranial length and low parietal subtense,
against Neanderthals they were primarily low supraorbital
projection, low frontal fraction, high parietal chord, high frontal
chord, low frontal subtense and low vertex radius, while against
Zhoukoudian Homo erectus they were low supraorbital projection,
high parietal chord, high bifrontal breadth, high vertex radius,
high frontal chord and low frontal subtense. Overall it appeared
that the cranium was ‘‘modern’’ in its low supraorbital projection,
and long frontal and parietal chords, but ‘‘archaic’’ in its high
cranial length, low vertex radius, and low frontal and parietal
subtenses. Stringer’s results highlighted apparent archaic aspects in
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the specimen in its long and rather low cranial shape, and
although modern overall, it also resembled fossils such as Omo
Kibish 2, Saccopastore 1 and Ngandong in several respects, falling
closer to them than to Upper Palaeolithic and recent samples in
some analyses (Figure 2).
In light of the redating of the LSA to a much deeper time depth
than originally thought, and of the scarcity of LSA human skeletal
remains from Africa in general and from West Africa in particular,
we undertook a renewed study of the Iwo Eleru cranium with the
aim of better determining its affinities and geological age [4,5]. A
Figure 1. Map of Nigeria, showing the geographic location of the Iwo Eleru rockshelter, and the Iwo Eleru calvaria. Clockwise from top
left: Lateral, frontal, ventral and superior views.
doi:10.1371/journal.pone.0024024.g001
Figure 2. Visualization of the results of Stringer’s multivariate analyses [2,3], showing the position of the Iwo Eleru calvaria. Mutually
close specimens are joined by lines, but an arrowed line indicates where the proximity is not mutual. For example Saccopastore is a nearest
neighbour to Petralona, but Petralona is not a near neighbour of Saccopastore. Redrawn with permission from [3].
doi:10.1371/journal.pone.0024024.g002
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primary replica of the cranial vault of the Iwo Eleru specimen,
produced before its return to Nigeria, was digitized by one of the
authors (KH). Comparisons of Stringer’s measurements on the
original and the replica show a maximum discrepancy of 1 mm,
suggesting the replica accurately reflects the original shape of the
cranium. The 3-D coordinates collected were included in an
extensive comparative dataset of Middle, Late Pleistocene and
Holocene humans, and a multivariate statistical analysis was
undertaken with the goal of assessing its affinities and phylogenetic
/ population relationships in the context of geographic and
temporal human cranial variation. Furthermore, in order to check
the possibility that the associated radiocarbon age did not date the
specimen, one of us (AF) provided a long bone cortical fragment
approximate 1 cm square for a new age estimate. Unfortunately
the lack of collagen prevented a direct radiocarbon determination
at the Oxford Radiocarbon Accelerator, so Uranium-Series dating
of the fragment was carried out instead.
Results
Morphometric analysis
The results of the principal components analysis (PCA) were
similar to those described previously for similar neurocranial
datasets analyzed by one of us (KH; Figure 3; [6–8]). The first
principal component accounted for 32.4% of the total variance
and separated archaic from modern human specimens. The two
H. erectus (s.l.) specimens fell at the extreme negative of this axis,
followed by Neanderthals and H. h eide lbe rge nsis (s.l.). Modern
human populations were characterized by more positive scores
on PC 1, and there was only minimal overlap among their 95%
confidence ellipses and that of the Neanderthals. The Middle-
Late Pleistocene African specimens (LH 18, Singa, Djebel
Irhoud 1 and 2) and the early modern human specimens from
Qafzeh and Skhul fell in the intermediate zone between
Neanderthals / H. heidelbergensis on one hand and modern
humans on the other. Qafzeh 9 was the exception, falling on the
positive end of PC 1 and close to Upper Paleolithic European
specimens. The latter sample, which included some of the
earliest modern human specimens in Europe (Mladec
ˇ
1and5,
Oase 2, Muierii 1, Cioclovina), clustered within the modern
human range of variation, and not in the zone of overlap with
the archaic specimens. One of the two specimens from
Zhoukoudian Upper Cave (UC 101) had a more negative PC
1scoresimilartothatofQafzeh6andJebelIrhoud2(seealso
[8]). Iwo Eleru showed a similarly negative PC 1 score, falling
closest to LH 18, Saldanha (Elandsfontein) and Spy 2 along this
axis. PC 1 reflected differences in the shape of the neurocranium
from an elongated, low vault and large, evenly thick,
supraorbital torus to a rounded, antero-posteriorly shorter vault,
and thinner supraorbital torus with differentiated medial and
lateral segments.
PC 2 (11.3% of the total variance, Figure 3) appeared to reflect
variation among modern humans, with the sub-Saharan African,
the Khoisan, Oceanic and Upper Paleolithic samples clustering
around zero, and on the positive end of this axis. The Andaman
sample was restricted to the negative side, while the Inuit fell
around zero. The Europeans, N. Easterners, Asians and
Iberomaurusians spanned the entire length of PC 2. The LPA
sample was also quite spread out along this axis, while the
Neanderthals, H. erectus and H. heidelbergensis s.l. were relatively
centered around zero and on the negative side. Iwo Eleru was
once more placed closest to LH 18 and Saldanha. Crania with
relatively negative scores on PC 2 displayed antero-posteriorly
short and medio-laterally wide shapes, while those with positive
scores showed antero-posteriorly long and medio-laterally narrow
vaults.
Iwo Eleru generally showed large distances to the other
specimens in this analysis. It displayed the shortest inter-individual
Procrustes distance to LH18 (0.080), and next closest to La
Chapelle-aux-Saints (0.087) and a recent Australian (0.089). LH18
itself was closest to the Middle Pleistocene Saldanha individual
(0.059). It also showed relatively small Procrustes distances to two
Upper Paleolithic Europeans, Oase 2 (0.071) and Predmostı
´
3
(0.074). La Chapelle showed the shortest distances to other
Neanderthals: Guattari (0.054), La Quina 5 (0.054), Spy 1 (0.057),
Amud 1 (0.061), La Ferrassie 1 (0.067), Feldhofer 1 (0.075),
Shanidar 1 (0.076); as well as to older specimens: Sima de los
Huesos Cranium 5 (0.069), Dali (0.060), Irhoud 1 (0.067). The
Procrustes inter-individual distances were used to generate a
minimum spanning tree for the fossil specimens on the plot of PC
1 and 2 (Figure 3).
The results of the canonical variates analysis (CVA) were
consistent with those of the PCA (Figure 3). The first canonical
axis (49.7%) separated archaic from modern specimens, with late
archaic or early modern humans (the Irhoud specimens, Qafzeh 6,
Singa, LH18) generally falling in an intermediate position. Iwo
Eleru, as well as Upper Cave 101, also fell in this region, with the
former and LH18 being just at the outskirts of the Neanderthal
confidence ellipse. The Mahalanobis squared distances among the
predefined groups are reported in Table S2. Iwo Eleru showed
large distances from all other groups. The smallest distance was to
the Upper Cave specimens, themselves a very small group of just
two individuals. Relatively small squared distances were also
shown between Iwo Eleru and the Qafzeh-Skull group, Neander-
thals and H. erectus (s.l.).
The departure of Iwo Eleru from the modern human average
cranial shape was further underlined by the comparison of its
landmark configuration to the mean configuration of modern
humans (Figure 4A). Iwo Eleru was characterized by a more
elongated cranial vault and flattened frontal and parietal bones. Its
browridge was also slightly more forward projecting than the
average modern human shape. Iwo Eleru was more comparable to
the mean LPA landmark configuration in its elongated and low
cranial shape and the degree of browridge projection (Figure 4B).
Its nearest recent human neighbor, an Australian female
(Figure 4C), also showed a relatively low vault and pronounced
browridges. However, the latter specimen exhibited an overall
more curved sagittal profile than Iwo Eleru, with a more steeply
rising frontal bone, an expanded and more curved parietal and a
more rounded occipital with a lower position of inion, all typical
modern human conditions.
Uranium-Series Dating
The elemental U and Th values vary greatly along the profiles
of the bone sample from the Iwo Eleru skeleton (left-hand
diagrams in Figures S1 and S2). The outer surfaces and pores
show measureable Th concentrations, which indicate the presence
of detrital material. There is a gradient of higher U-concentrations
in the centre of the bone (around 80 to 100 ppm) towards the
outsides where U-concentrations of 50 to 60 ppm were measured.
These lower U-concentrations may either be due to a denser bone
structure, with less internal surface area for adsorbing uranium, or
to leaching of U from the volumes close to the surface. The
apparent U-series age estimates vary between about 10 to 14 ka in
the central part of the bone and increase in some laser scans to
between about 15 to 17 ka closer to the surface. The right-hand
columns of Figures S1 and S2 show the plot of apparent U-series
age versus U-concentration.
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Figure 3. Results of the multivariate statistical analysis of landmarks and semilandmarks. Top: Principal components analysis, PC1 and 2.
Cranial shape differences along PC 1 are shown below the graph. The top graph shows a Minimum Spanning Tree of the Inter-individual Procrustes
distances for the fossil specimens (black lines connecting specimens). Specimen labels as in Table 1. Bottom: Canonical variates analysis, CV 1 and 2.
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It is expected from the diffusion-adsorption model for U-
uptake [9–12] that spatially resolved analyses across a homoge-
neous bone yield u-shaped or constant U-concentration and
apparent U-series age profiles. In ideal circumstances, a plot of
apparent U-series age versus U-concentration would either be flat
or show increasing U-series age estimates with increasing U-
concentrations. This is clearly not the case for the results on Iwo
Eleru (Figures S1 and S2, right hand columns). The apparent U-
series age estimates are more or less constant in the inner part of
the bone fragment and increase towards the outside while the U-
concentrations decrease.
One of the problems of U-series dating of bone is that the
different domains within a bone may give very different U-series
ages. The best age estimate is actually not derived by simply
averaging all results, but from identifying the domains that had
experienced the fastest U-uptake and have remained a closed
system since. This may only apply to very small volumes (see [13]).
The U-series analyses of the central part of the bone give a
minimum age of the sample. Excluding any results with more than
10 ppb Th (indication of contamination) and U concentrations of
less than 75 ppm, all scans give compatible results with mean ages
ranging between 10.661.7 (Track 2) and 12.761.6 ka (Track 4),
see right hand columns in Figures S1 and S2. Most apparent U-
series age results from the central parts of the bone are within 9
and 14 ka. Virtually all age results overlap within their errors.
Most of the scatter is likely due to statistical variation. The best age
estimate is thus derived from the mean value of all Th-free age
estimates in the central part of the bone (11.761.7 ka). This age
estimate is derived from more than 80% of the exposed bone area
(excluding the pores), which may be taken as an indication that
most of the uranium was accumulated within a relatively short
time range. The average U-series age increases by less than 1 ka
(i.e. less than 10%) by including the Th-free results of the domains
with lower U-concentrations. Considering that the outer U-
concentrations are lower by up to a factor of four compared to the
interior part, U-leaching is apparently not the main cause for the
reduced U-concentrations.
The question is whether the specimen could be substantially
older. Most older apparent age estimates are associated with
relatively high Th and low U concentrations, either close to the
outside or in pores (Tracks 1, 3, 4, 11, and 12). Here, the older
apparent U-series results may well have been influenced by detrital
material as well as U-leaching. Other older results (.15 ka) are seen
for example in Track 8 (around cycle 3100), Track 11 (around cycle
430 and 550) and Track 12 (around cycle 1480), see arrows in the
respective diagrams in Figure S2. In Track 12, the section between
cycle 1481 and 1488 yields an age of 19.361.8 ka. The immediately
adjacent sections yield 13.962.6 ka (cycles 1472 to 1481) and
10.862.1 ka (cycles 1488 to 1505). It is a simple statistical fact that
some subsamples of a single population will deviate from the other
results by more than 2-s. The most likely apparent age result comes
from the average of this section. The same seems to apply to the
other marked sections.
Nevertheless, Tracks 9 (between cycles 3076 and 3161) and 11
(between cycles 726 and 791, see circles in the respective
diagrams of Figure S2) show wider domains with relatively old
apparent U-series ages (15.061.3 and 16.360.5 ka), which do
not depend on the U-variations within these domains. While U-
leaching cannot entirely be excluded in these sections, the lower
U-concentrations may just as well be due to different amounts of
internal surface area. These two sections are close to the lower
surface and could have preserved the original U-series isotope
signatures. If this is the case, the most likely age of the bone is
around 16.3 ka. In summary, the minimum age of the bone is
around 11.761.7 ka while some domains indicate an age as old
as 16.360.5 ka.
Symbols: Grey diamonds. Modern humans; Black up triangles: Upper Paleolithic modern humans; Purple up triangles: Late Pleistocene African and
Near Eastern hominins; Red stars: H. neanderthalensis; Red squares: H. heidelbergensis (s.l.); Black squares: H. erectus (s.l.). Ellipses indicate 95%
confidence ellipses for Neanderthals (red) and modern humans (gray).
doi:10.1371/journal.pone.0024024.g003
Figure 4. Shape comparisons of Iwo Eleru. Iwo Eleru (black)
compared to the modern human mean configuration (A, gray), to the
Late-Middle Pleistocene African mean configuration (B, gray), and to its
closest modern human neighbor in overall shape (C, gray).
doi:10.1371/journal.pone.0024024.g004
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Discussion
Our analysis indicates that Iwo Eleru possesses neurocranial
morphology intermediate in shape between archaic hominins
(Neanderthals and Homo erectus) and modern humans. This
morphology is outside the range of modern human variability in
the PCA and CVA analyses, and is most similar to that shown by
LPA individuals from Africa and the early anatomically modern
specimens from Skhul and Qafzeh. Iwo Eleru is distinct from the
recent African samples used here (although the range of recent
modern human variation encompasses relatively low and elongated
cranial shapes approaching this condition). Past work has suggested
that neurocranial shape reflects population history relatively reliably
among modern human populations [14,15]. Although we did not
find unambiguous strong affinities between Iwo Eleru and the
samples used here, its overall morphological similarities with early
modern humans suggest a link to these early populations and
possibly a late Middle-early Late Pleistocene chronology. Nonethe-
less, the archaeological setting, stratigraphy, previous radiocarbon
[see 4] and our new U-series dating indicate a much younger,
terminal Pleistocene age for this cranium. Such a late chronology for
the Iwo Eleru cranium implies that the transition to anatomical
modernity in Africa was more complicated than previously thought,
with late survival of ‘‘archaic’’ features and possibly deep population
substructure in Africa during this time.
Thus our restudy of the Iwo Eleru cranium confirms previously
noted archaic cranial shape aspects, and the U-series age estimates
on its skeleton support the previously proposed terminal Pleistocene
date for this burial. Our findings also support suggestions of deep
population substructure in Africa and a complex evolutionary
process for the origin of modern humans [16,17,7,18,19,20,21].
Perhaps most importantly, our analysis highlights the dearth of
hominin finds from West Africa, and underscores our real lack of
knowledge of human evolution in that region, as well as others. As
also indicated by restudy of the Ishango (Congo) fossils [22], Later
Stone Age fossils from at least two regions of Africa retain significant
archaic aspects in their skeletons. We hope that the next stage of this
research will extend studies to the Iwo Eleru mandible and
postcrania, and to comparative materials such as those from Ishango.
Materials and Methods
Morphometric analysis
The comparative sample for this analysis comprises several
Pleistocene human fossils from Africa and Eurasia, and two
hundred and forty two recent human crania representing nine
broad geographic groups (Tables 1 and 2). The sex of the modern
human crania was assigned on the basis of museum catalogue
records, cranial morphology and size and, in the rare cases of
associated postcrania, pelvic morphology. In as much as possible,
male and female samples were balanced for sample sizes. Since
such sex assignment is imperfect for recent humans, and even
more problematic for fossil specimens, sexes were pooled in the
analyses. Original fossils were measured, with the exception of few
cases where the originals no longer exist or were unavailable for
study. In those few instances, high quality casts or stereolitho-
graphs from the collections of the Division of Anthropology of the
American Museum of Natural History, the Department of
Anthropology at New York University, the Institut de Pale´onto-
logie Humaine, and the Department of Human Evolution at the
Max Planck Institute for Evolutionary Anthropology, were
measured. Using casts as alternatives to fossil specimens is an
imperfect solution but one that is necessary in cases where the
originals are not available for study, or have been destroyed.
Data were collected in the form of three-dimensional coordinates
of neurocranial osteometric landmarks, defined as homologous
points that can be reliably and repeatedly located, using a
Microscribe [23] portable digitizer (Table S1). Landmarks along
the midsagittal profile from glabella to inion, along the coronal and
lambdoid sutures, and along the upper margin of the supraorbital
torus were also registered (Table S1). The points along these outlines
were automatically resampled to yield the same semilandmark
count on every specimen [24,6]. These points were chosen so as to
reflect the neurocranial morphology of the fossils as fully as possible.
The data were processed using geometric morphometric
methods (GMM), which preserve the geometry of the object
studied better than traditional measurements, and thus allow for a
better analysis of shape. These techniques also readily account for
size correction and enable visualization of the shape changes
between specimens in specimen space. Perhaps most importantly,
they allow the quantification of some anatomical features that are
difficult to measure conventionally. Because of these qualities,
GMM have gained widespread and increasing use in the recent
literature on human variation. Despite these general advantages of
GMM, they do not accommodate missing data, often necessitating
some level of data reconstruction in fossil studies. Therefore
landmarks on specimens with minimal damage were estimated
during data collection, using anatomical clues from the preserved
surrounding areas. Bilateral landmarks and curves missing on one
Table 1. Fossil comparative samples used in the analysis.
European – W. Asian H. neanderthalensis (n = 10; NEA)
Amud 1 (Am1), Feldhofer 1* (Fh1), Guattari (Gt) La Chapelle-aux-Saints (Ch), La Ferrassie 1 (Fr1), La Quina 5 (Qn), Shanidar 1* (Sh1), Spy 1& 2 (Sp1, Sp2), Tabun 1 (Tb1)
Homo heidelb ergensis s.l. (n = 5; HH)
Dali* (Da), Kabwe (Broken Hill) (Kb), Petralona (Pe), Saldanha (Elandsfontein) (Sl), Sima de los Huesos 5* (Sm5)
Homo erectus s.l. (n = 2; HE)
KNM-ER 3733 (ER3733), KNM-ER 3883 (ER3883)
Late Middle-Late Pleistocene fossils from Africa and the Levant (n = 7; LPA, EAM)
Irhoud 1& 2 (Ir1, Ir2), Ngaloba (LH18), Qafzeh 6* & 9 (Qz6, Qz9), Singa (S1), Skhul 5 (Sk5)
Upper Paleolithic Eurasian modern humans (n = 20; EUP), Zhoukoudian Upper Cave (n = 2; UC)
Abri Pataud (AP), Brno 1 (Bn1), Chancelade (Cn), Cioclovina (Ci), Cro Magnon 1, 2, 3 (CM1, CM2, CM3), Dolnı
´
Ve
ˇ
stonice 3, 13, 15, 16 (Dv3, Dv13, Dv15, Dv16), Grimaldi 4*
(Gr), Mladec
ˇ
1, 5 (Ml1, Ml5), Muierii (Mu), Oase 2 (Oa), Ohalo II* (Oh2), Pavlov (Pv), Pr
ˇ
edmostı
´
3*, 4* (Pd3, Pd4), Upper Cave 101* &103 * (UC1, UC3)
*Indicates specimens for which high-quality casts or stereolithographs were measured. The symbols for each specimen used in the Figures are indicated in parentheses.
One of the authors (Stringer) regards Sima de los Huesos 5 as an early Neanderthal rather than a H. heidelbergensis.
doi:10.1371/journal.pone.0024024.t001
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side were further reconstructed by superimposing the landmark
configurations of specimens with missing data with their
reflections, and by substituting the coordinates for each missing
landmark with the fitted homologous counterpart on the other
side. This is a process known as ‘reflected relabeling’ [25]. Further
data reconstruction was allowed in the case of LH 18, an
important specimen with only minimal damage (frontomalare
temporale is missing on both sides). Semilandmarks were ‘slid’ in
Mathematica [26] using routines developed by Philipp Gunz and
Philipp Mitteroecker [27]; for additional details see also [28,6].
Landmarks and slid semilandmarks were superimposed with
Generalized Procrustes Analysis (GPA) using the Morpheus software
package [29]. The fitted coordinates were then analyzed statistically
using principal components analysis (PCA), canonical variates
analysis, Procrustes distances, and Mahalanobis squared distances.
These statistics were calculated with the software packages SAS [30],
NTSys [31], and TPSsmall (version 1.20; [32]). Visualization of
shape differences along principal components axes was achieved
with the use of the EVAN toolbox (EVAN society). The pattern of
variation in the sample was evaluated through the PCA, and the
similarities among specimens were assessed using inter-individual
Procrustes distances (defined as the square root of the sum of squared
distances between two superimposed landmark configurations).
Similarities and differences among groups were evaluated using
the CVA, Mahalanobis D
2
and mean Procrustes distances between
groups. For the purposes of these analyses the fossil samples were
partitioned in the following groups: H. neanderthalensis (NEA); H.
heidelbergensis sensu lato; Late Pleistocene Africans (LPA); Early
anatomically modern humans from Qafzeh and Skhul (EAM);
Upper Paleolithic Europeans (EUP); and Zhoukoudian Upper Cave
101 and 103 (UC). The Mahalanobis statistic represents the
morphological difference among groups, scaled by the inverse of
the pooled within-group covariance matrix. The larger the values of
the D
2
distance, the farther the group centroids are from each other.
Mahalanobis D
2
assumes equality of covariance, and therefore
might be affected by violations of this assumption (though see [33]
for a discussion of this issue). Procrustes distance, on the other hand,
does not account for non-independence of landmark coordinates
and within-group variation. It reflects differences in total shape, and
does not take into account patterns of covariation. It is therefore not
affected by the assumption of equality of covariance. The first 15
principal components (all components accounting for .0.1% of the
total variance; taken together they account for 82.4% of the
variance) were used as variables in the CVA and Mahalanobis
analyses in order to reduce the number of variables. Because sample
sizes were not equal, a correction in calculating this statistic was used,
following [34]. Finally, morphological similarity was assessed visually
by comparing the landmark configuration of Iwo Eleru, after size
correction, to the mean landmark configurations of other groups,
using the software package Morpheus [25].
Uranium-series analysis
In order to obtain an age estimate on the human remains from
Iwo Eleru, a postcranial bone was directly analysed for dating. A
diamond wire saw was used to cut a plane cross section about 2 mm
away from the surface. The central part of the bone shows large
pores which are filled with detritus. The upper 2 mm contain many
smaller pores while the lower 1.5 to 2 mm consist of dense bone with
few, small pores. Twelve laser ablation scans were then recorded on
the cross-section (Figure S3), with the scan direction perpendicular to
the outer surfaces. Laser ablation U and U-series analyses were
carried out at Australian National University; for the experimental
set-up see [35,36] and for applications on human fossils [37,38,13].
Supporting Information
Figure S1 Summary of elemental and U-series analysis for
Tracks 1 to 6. Left hand panels: U, and Th elemental
concentrations and age calculations. Right hand panels: Relation-
ship between calculated age and U-concentration.
(TIF)
Figure S2 Summary of elemental and U-series analysis for
Tracks 7 to 12. Left hand panels: U, and Th elemental
concentrations and age calculations. The age results indicated by
arrows and circles are discussed in the text. Right hand panels:
Relationship between calculated age and U-concentration.
(TIF)
Figure S3 Cross section of the bone sample used for laser
ablation U and Th elemental as well as U-series analysis. Arrows
indicate the position of the scans shown in Figures S1 and S2.
(TIF)
Table S1 Landmarks and semi landmarks used in the analysis
(DOCX)
Table S2 Mahalanobis D
2
among groups used in this study.
Below the diagonal are values corrected for unequal sample sizes.
Sample labels as in Tables 1 and 2.
(DOCX)
Acknowledgments
We thank NHM Curator Robert Kruszynski for access to and loan of the
cast of the Iwo Eleru calvaria, Philipp Gunz for processing the semiland-
mark data, Tom Higham RLAHA Oxford for the unsuccessful direct
radiocarbon dating attempt, Silvia Bello for redrawing the map and figure
2, and the NHM Photo Unit. This is NYCEP morphometrics group
contribution Nr. 59.
Author Contributions
Conceived and designed the experiments: KH CS. Performed the
experiments: KH CS RG MA PA-J CAF. Analyzed the data: KH RG
MA. Wrote the paper: KH CS RG MA PA-J CAF.
Table 2. Recent human comparative samples.
Recent human samples
Sub-Saharan African (AFR; Kenya, Zulu; sub-recent; NHM, WITS) n =27
Andamanese (AND; Andaman Islands; sub-recent; NHM) n =28
Asian (AS; China, Thailand; sub-recent; MH) n =39
Oceanic (OCE; Australia; sub-recent; NHM) n =26
Khoisan (KHO; South Africa; Holocene; IZCT, UCT) n =58
Inuit (IN; Alaska, Greenland; sub-recent; AMNH) n =14
Europe (EUR; sub-recent; IAL) n =15
Near East (NE; Syria; sub-recent; MH) n =20
Iberomaurusian (IB; Morocco; Holocene; IPH) n =15
Total n = 242
Museum abbreviations: AMNH: American Museum of Natural History, New York;
IAL: Institute of Anatomy, Leipzig; IPH: Institut de Pale
´
ontologie Humaine, Paris;
IZCT: Iziko Museums of Cape Town; MH: Muse
´
edel9Homme, Paris; NHM:
Natural History Museum, London; UCT: University of Cape Town; WITS:
University of the Witwatersrand, Johannesburg.
The population labels used in the Figures, the geographic and temporal
provenience of the samples, and the museums where these samples are housed
are indicated in parenthesis.
doi:10.1371/journal.pone.0024024.t002
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