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Homo antecessor: The state of the art eighteen years later
Jos
e-María Bermúdez-de-Castro
a
,
*
, María Martin
on-Torres
a
, Laura Martín-Franc
es
a
,
Mario Modesto-Mata
a
, Marina Martínez-de-Pinillos
a
, Cecilia García
a
,
Eudald Carbonell
b
,
c
a
Centro Nacional de Investigaci
on sobre la Evoluci
on Humana (CENIEH), Paseo de la Sierra de Atapuerca 3, 09002, Burgos, Spain
b
Institut Catal
a de paleoecologia Humana I Evoluci
o Social (IPHES), Marcel.li Domingo s/n, 43007, Tarragona, Spain
c
Laboratory of Human Evolution, Institute of Vertebrate Paleontology and Paleoanthropology (IVPP), Chines Academy of Sciences, 100044, Beijing, China
article info
Article history:
Available online xxx
Keywords:
Human evolution
Homo antecessor
Sierra de Atapuerca
Gran Dolina
abstract
It is eighteen years since the human fossils recovered from the TD6 level of the Gran Dolina cave site, in
Sierra de Atapuerca (Burgos, northern Spain) were assigned to a new hominin species, Homo antecessor.
This review summarizes the main results obtained from the study of these fossils during this period. The
increase of the African and Eurasian fossil record, as well as the application of new methodological
approaches, has led to competing interpretations about its hypothetical phylogenetic position and
possible evolutionary scenarios. At present, we can argue that this species is defined by a unique mosaic
of primitive traits for the Homo clade, a certain number of derived features present in modern humans, a
significant suite of derived features shared with Neandertals and their ancestors in the European Middle
Pleistocene (in particular with the Atapuerca-Sima de los Huesos hominins), and some derived features
shared with the Chinese Middle Pleistocene hominins. From this evidence, we suggest that a speciation
event could have occurred in Africa/Western Eurasia, originating a new Homo clade. Homo antecessor,
most probably dated to the MIS 21, could be a side branch of this clade placed at the westernmost region
of the Eurasian continent.
©2015 Elsevier Ltd and INQUA. All rights reserved.
1. Introduction
During the 1994 and 1995 field seasons, an assemblage of near
ninety human fossil remains and about 150 Mode 1 artifacts were
recovered from the so-called Aurora stratum of the TD6 litostrati-
graphic unit (LU) of the Gran Dolina cave site in Burgos (Fig. 1),
northern Spain (Carbonell et al., 1995, 1999). These findings
occurred during the excavation of an archaeological test pit of about
six square meters, made in order to evaluate the potential of the
site. The first paleomagnetic studies revealed the presence of the
Matuyama/Bruhnes reversal at the top of the TD7 LU, about 117 cm
(cm) above the Aurora stratum (Par
es and P
erez-Gonz
alez, 1995,
1999). The study of these human fossils evinced a unique combi-
nation of primitive and derived features regarding the Homo clade,
and we proposed a new Homo species, H. antecessor (Bermúdez de
Castro et al., 1997).
It has been nearly 18 years since this proposal. In this period,
another sixty human fossils were obtained in TD6 from a small area
near the test pit made during the nineties of the twentieth century.
During this excavation, the stratigraphic sequence of TD6 was
refined (see Bermúdez de Castro et al., 2008a,b and Figs. 2 and 3)
and new additional geochronological information is available from
the Gran Dolina site (see below). Furthermore, new studies have
been made from the TD6 human fossils. These studies, the finding
of new African and Eurasian human remains (e.g. Abbate et al.,
1998; Manzi et al., 2001; Asfaw et al., 2002; Gabunia et al., 2002;
Macchiarelli et al., 2004; Lumley and Lordkipandize, 2006;
Carbonell et al., 2008; Kappelman et al., 2008; Carretero et al.,
2009; Krause et al., 2010; Vialet et al., 2010; Bermúdez de Castro
et al., 2011; Roksandic et al., 2011; Liu et al., 2013; Toro-Moyano
et al., 2013; Arsuaga et al., 2014; Xing et al., 2014, 2015)aswellas
the reinterpretation of specimens recovered in the past (e.g. Manzi
et al., 2003; Mounier et al., 2009; Manzi et al., 2010; Stringer, 2012;
Liu et al., 2013) have offered a considerable amount of information
to reconsider our first proposal and to look for alternative and
*Corresponding author.
E-mail addresses: josemaria.bermudezdecastro@cenieh.es (J.-M. Bermúdez-de-
Castro), maria.martinon@cenieh.es (M. Martin
on-Torres), laura.martinfrances@fa.
cenieh.es (L. Martín-Franc
es), mario.modesto@cenieh.es (M. Modesto-Mata),
marina.martinezdepinillos@cenieh.es (M. Martínez-de-Pinillos), cecilia.garcia@
cenieh.es (C. García), valtes@iphes.cat (E. Carbonell).
Contents lists available at ScienceDirect
Quaternary International
journal homepage: www.elsevier.com/locate/quaint
http://dx.doi.org/10.1016/j.quaint.2015.03.049
1040-6182/©2015 Elsevier Ltd and INQUA. All rights reserved.
Quaternary International xxx (2015) 1e10
Please cite this article in press as: Bermúdez-de-Castro, J.-M., et al., Homo antecessor: The state of the art eighteen years later, Quaternary
International (2015), http://dx.doi.org/10.1016/j.quaint.2015.03.049
possibly complementary hypotheses (e.g. Bermúdez de Castro et al.,
2003; Martin
on-Torres et al., 2007; Bermúdez de Castro et al.,
2008a,b; Endicott et al., 2010; Martin
on-Torres et al., 2011;
McDonald et al., 2012; Bermúdez de Castro and Martin
on-Torres,
2013).
In this review, we present a summary of the main results
presented so far about the TD6 hypodigm, as well as the different
interpretations made on the meaning of these hominins in the
context of the African and Eurasian human evolution. It is
important to note that a certain number of new analyses of the
TD6 hominins are in progress, which undoubtedly will offer
additional information to test our hypothesis. Furthermore, in a
near future the present Atapuerca Research Team will have ac-
cess to a wide area of the different thin sublevels forming the
Aurora archaeostratigrafic set (also named TD6-2). This will be an
opportunity to increase our knowledge of this hominin popula-
tion, who lived in Western Europe during the late Early
Pleistocene.
2. The TD6 level
The Gran Dolina cave site (TD) fills up a large cavity about 27 m
deep and with a maximum width of 17 m (see Fig. 3 in Bermúdez de
Castro et al., 2013). The stratigraphic section of the site was cut and
exposed by the construction of a railway trench. Gil and Hoyos
(1987) divided this section from bottom to top into eleven levels:
TD1 to TD11. However, the stratigraphy of the Gran Dolina site is
under continuous refinement. There is a vertical cut of the section
in progress, (e.g. Bermúdez de Castro et al., 2008a). In addition, we
are currently studying a wide pit about 10 m deep excavated below
the present level of the ancient railway (see Fig. 1). Par
es and P
erez-
Gonz
alez (1995, 1999) observed a polarity reversal between TD7
and T8, interpreted as the Matuyama/Brunhes boundary, meaning
that levels TD8eTD11 were deposited during the Middle Pleisto-
cene, whereas levels TD7eTD1 were attributed to the Early Pleis-
tocene. This finding is consistent with the change in the fossil
record of large- and micromammals, with a transition in TD6-2
(Faunal Unit 4), TD7eTD8 (Faunal Unit 5) and drastic change in
TD9eTD11 (Faunal Unit 6) (Cuenca-Besc
os and García, 2007;
Cuenca-Besc
os et al., 2010). Pollen analysis of TD6 (García-Ant
on,
1989) suggests a Mediterranean climate for this level, whereas
the study of the amphibian and squamate reptile fossil record (Blain
et al., 2009) of TD6-2 also suggests a slightly warmer temperature
than today in Burgos.
The combination of paleomagnetic data and USeESR ages
suggest a range between 0.78 and 0.86 Ma (million years ago) for
TD6-2 (Falgu
eres et al., 1999). Thermoluminescence (TL) ages
(Berger et al., 2008) on samples taken 1 m below the Brunhes/
Matuyama boundary (0.78 Ma) give an age of 0.96 ±0.12 Ma for
TD6, which may correspond to MIS 25. The last systematic
dating of the Gran Dolina sequence has been made by Moreno
(2011) using the ESR dating method on optically bleached
quartz. This author analysed six samples for TD6 and TD7,
obtaining an age range of 0.80e0.88 Ma for these levels, which is
consistent with the biostratigraphic and paleomagnetic analyses
and suggest that the human assemblage was deposited during
MIS 21.
Fig. 1. The Gran Dolina cave site is about 27 m deep. The lower two thirds of the
sequence belong to the Lower Pleistocene. A test pit made between 1993 and 1999, as
well as a vertical cut of the entire sequence allowed to found the human fossils from
the TD6 level (see arrow and Fig. 2).
Fig. 2. Upper sequence of the lithostratigraphic unit TD6 from the Gran Dolina cave
infilling (Matuyama Chron), which includes the ‘‘Aurora archaeostratigraphic set’’
(AAS), also known as TD6-2. All the human fossils of the H.antecessor hypodigm have
been recovered from this section of the unit TD6. The AAS is not well defined as a
sequence of different layers on the test pit performed in the 1994e1996. Thus, the AAS
corresponds to what was named “Aurora stratum”during the first excavations
(Carbonell et al., 1995). Modified from Bermúdez de Castro et al., 2008a).
J.-M. Bermúdez-de-Castro et al. / Quaternary International xxx (2015) 1e102
Please cite this article in press as: Bermúdez-de-Castro, J.-M., et al., Homo antecessor: The state of the art eighteen years later, Quaternary
International (2015), http://dx.doi.org/10.1016/j.quaint.2015.03.049
3. Materials and methods
3.1. The TD6 human remains
The human remains from TD6b are in good preservation,
although the majority of them are fragmentary due to clear events
of cannibalism (Fern
andez-Jalvo et al., 1999; Carbonell et al., 2010).
Nevertheless, we recorded and analyse a number of cranial and
postcranial features, mainly from the teeth, the mandibles and the
face. Postcranial remains are also numerous and represent different
anatomical elements, including nearly twenty-five hand and foot
remains.
In this synthetic review we provide an overview of the infor-
mation obtained from the study of the different cranial, and post-
cranial features observed in H.antecessor, carried out by Arsuaga
et al. (1999), Carretero et al. (1999), Lorenzo et al. (1999), Rosas
et al. (1999), Carbonell et al. (2005), Bermúdez de Castro et al.
(2008a,b), Bermúdez de Castro et al. (2012) and Pablos et al.
(2012). Concerning teeth, their crown and root morphology have
been analysed in previous studies (Bermúdez de Castro et al., 1997;
Bermúdez de Castro et al., 1999; Bermúdez de Castro et al., 2003;
Carbonell et al., 2005; Bermúdez de Castro et al., 2008a,b;
Martin
on-Torres et al., 2006, 2007;G
omez-Robles et al., 2007,
2008, 2011, 2011, 2012).
3.2. Minimum number of individuals (MNI)
In previous studies we assessed the possible minimum number
of individuals (MNI) currently represented in the TD6 hypodigm
(e.g. Bermúdez de Castro et al., 2006). However, due to the
considerable fragmentation of the hominin remains, this aspect
remains difficult. Furthermore, the six sublevels (generally less than
10 cm) identified during the last excavations (Bermúdez de Castro
et al., 2008a,b) are condensed near the wall of the cave, where the
test pit was made during the nineties. Then, it was not possible to
state the precise provenance of each of the human remains found in
the test pit in correlation with the six levels, which were deposited
in at least two different time events. Although we suspect that the
MNI is higher than the estimation presented in Table 1, in this paper
we prefer to be conservative and to avoid speculations with the
association of some isolated permanent and deciduous specimens.
The present TD6 hypodigm includes four isolated deciduous teeth,
two permanent Incisive germs and two permanent complete lower
incisors, some of which could represent additional immature or
adult individuals. Summarizing, and considering that we have
excavated only a small area of the TD6 level, our conclusions on the
MNI are preliminary, except for the remarkable presence of a high
percentage of immature individuals in the TD6 hypodigm (75%). The
age at death of the individuals presented in Table 1 is only an
indicative approach. We have used modern human standards with
the aim of determining the MNI, but we are aware that this model
may not apply for this Early Pleistocene population.
Fig. 3. Vertical cut of the Gran Dolina site, pointing the position of the TD7, TD6, and TD5 levels. The scaffold is placed in the hollow left by the test pit made between 1993 and 1999.
Table 1
List of the individuals represented in the TD6 hominin hypodigm.
Hominin Inventory number Specimen Age at death
a
H1 ATD6-1 Left lower C 13.5e14.5
ATD6-2 Left I
2
ATD6-3 Right P
3
ATD6-4 Right P
4
ATD6-5 Right mandible fragment with M
1
eM
3
in-situ
ATD6-6 Fragment of crown of right lower C
ATD6-7 Right P
3
ATD6-8 Right P
4
(continued on next page)
J.-M. Bermúdez-de-Castro et al. / Quaternary International xxx (2015) 1e10 3
Please cite this article in press as: Bermúdez-de-Castro, J.-M., et al., Homo antecessor: The state of the art eighteen years later, Quaternary
International (2015), http://dx.doi.org/10.1016/j.quaint.2015.03.049
4. Results of the main studies performed in the TD6 human
fossils
In Tables 2, 3, and 4 we present the state (primitive or derived)
of the main features identified so far in the TD6 hypodigm. The
state of these features is evaluated in relation to the Homo clade.
The finding that the TD6 hominins exhibit a sapiens-like mid-
facial morphology was surprising (Bermúdez de Castro et al., 1997;
see Table 2). Arsuaga et al. (1999) made the first detailed study of
the midface of the immature specimen ATD6-69 (H3). These au-
thors described this specimen as having a coronal orientation of the
infraorbital surface, an inferoposterior slope of this surface (with
the development of a canine fossa), arcing of the zygomati-
coalveolar crest, a forward position of the nasal aperture, and
associated anterior flexion of the maxillary surface near the nasal
aperture. This last feature suggests that nose was projecting in
ATD6-69. Arsuaga et al. (1999) conclude that the derived sapiens-
like midfacial topography of ATD6-69 is not present in early Homo
(i.e. H. habilis,H. rudolfensis) and H. ergaster (or African H. erectus).
Interestingly, ATD6-69 shows a modern human pattern of dental
development (Bermúdez de Castro et al., 1999b). Lacruz et al.,
(2013) have showed close similarities between ATD6-69 and
H. sapiens regarding the facial growth remodeling pattern. This
pattern is totally different from the presumed primitive pattern of
the Homo clade, observed in the specimen KNM-WT 15000.
Another subadult specimen, ATD6-38, which is similar in size and
shape to ATD6-69, also presents canine fossa (Arsuaga et al., 1999).
Furthermore, the adult specimen ATD6-58, represented by a left
Table 2
Derived features shared by H.antecessor with modern humans.
Face:ecoronal orientation of the infraorbital surface, inferoposterior slope of this surface (with the canine fossa), anterior flexion in the maxillary surface and
arcing of the zygomatico-alveolar crest, a projecting nose, and a zigomaxillary tubercle.
Face:emodern (H.sapiens) growth remodelling pattern.
Skull:econvex superior border of the temporal squama.
Maxilla: eanterior position and almost vertical trajectory of the incisive canal.
Table 3
Primitive features of H.antecessor regarding the Homo clade.
Lower premolars:ecomplex occlusal and root morphology, asymmetry of the crown, large talonid, and presence of cingulum.
Permanent upper and lower molars:M2>M1.
Permanent upper second molar: four well developed cusps.
Permanent molars: complex occlusal enamel crenulation pattern.
Mandible:
- position of the mental foramen.
- position of the lateral prominence.
- position of the mylohyoid line in relation to alveolar margin at M3 level.
- trajectory of the mylohyoid line in relation to alveolar margin.
- relief of the pterygoid fossa.
- intersection between mandibular notch and condyle.
Radius: absolutely and relatively long radial neck.
Table 4
Derived features shared by H.antecessor with Neandertals and Middle Pleistocene Atapuerca-SH hominins.
Mandible: presence of the medial pterygoid tubercle.
Mastoid region: small and minimally projecting mastoid process and the anteriorly obliterated digastric groove.
Permanent lateral upper incisors: marked shovel shaped (Eurasian pattern).
Permanent lower fourth premolars: reduced occlusal polygon.
Permanent upper first molar: rhomboidal and compressed occlusal polygon and a skewed external outline with a bulging protrusion of the hypocone.
Clavicle:eabsolutely very long (maximum length), relatively slender (low robusticity index), pronounced shaft curvature, and relatively small ephiphyses.
Humerus:elarge olecranon fossa and very thin medial and lateral pillars.
Talus:erelatively narrower trochlea (only shared with Neandertals).
Table 1 (continued )
Hominin Inventory number Specimen Age at death
a
ATD6-9 Left P
4
ATD6-10 Right M
1
ATD6-11 Left M
1
ATD6-12 Right M
2
H2 ATD6-14 Left maxillary fragment,with dcedm
1
in-situ 3.5e4.0
H3 ATD6-69 Maxilla and left zygomatic bone, including: left P
3
,M
1
, and unerupted M
2
, and right I
2
eM
1
10.0e11.0
H4 ATD6-125 Right P
4
13.5e14.5
H5 ATD6-94 Right M
1
about 6.0
ATD6-103 Right M
1
H6 ATD6-96 Left half mandible, including P
3
eM
3
in-situ About 17.0
H7 ATD6-113 Fragment of the left half of a mandible including M
2
and M
3
in-situ. About 17.0
H8 ATD6-112 Right part of the mandibular corpus, from the symphysis to the crypt of the M
2
3.5e3.9
a
In years, and according to modern human patterns of dental development (see Bermúdez de Castro et al., 1999).
J.-M. Bermúdez-de-Castro et al. / Quaternary International xxx (2015) 1e104
Please cite this article in press as: Bermúdez-de-Castro, J.-M., et al., Homo antecessor: The state of the art eighteen years later, Quaternary
International (2015), http://dx.doi.org/10.1016/j.quaint.2015.03.049
large zygomaxillary fragment, exhibits a remarkable canine fossa,
as well as a great zygomaxillary tubercle placed in a maxillary
position, that projects out about 3.3 mm (Arsuaga et al., 1999).
Finally, an adult small zygomaxillary fragment (ATD6-19) also
shows a zigomaxillary tubercle in the same position, which projects
out about 2.0 mm (Arsuaga et al., 1999). These authors suggest that
the zigomaxillary tubercle may be present in the Zhoukoudian
maxilla II. Thus, the Zhoukoudian and the TD6 hominins would
represent the unique presence of this facial feature prior to the Late
Pleistocene (Arsuaga et al., 1999). Furthermore, Vialet et al. (2010)
have identified a facial pattern in the Chinese Middle Pleistocene
specimens, Yunxian II and Nankin 1, that is similar to that presented
by modern humans. Regarding all these results and since the Af-
rican origin of our species seems to be undisputed for the majority
of paleoanthropologists, the presence of a modern-like human face
in H. antecessor has been the subject of interest of some other re-
searchers (e.g., Freidline et al., 2013). The latter made an interesting
theoretical ontogenetic study of the ATD6-69 face by means of 3D
geometric morphometric analyses, with reference data mainly
from Neandertals and modern humans. Freidline et al. (2013)
concluded that ATD6-69 exhibits a modern-like human midfacial
morphology, although their analyses placed ATD6-69 near the
margin of modern human variation and intermediate between the
modern humans and Middle Pleistocene human samples. Accord-
ing to these authors, the face of this individual would not have been
significantly altered in the course of the subsequent development.
Finally, and concerning the skull features, the TD6 hominins
share with Neandertals and modern humans a convex superior
border of the temporal squama, as well as an anterior position of
the incisive canal, which is nearly vertical (Arsuaga et al., 1999).
These authors also concluded that the TD6 hominins show a small
and minimally projecting mastoid process and the anteriorly
obliterated digastric groove, a feature shared with Neandertals
(Table 4).
Some of the mandibular features are primitive regarding the
Homo clade (Table 3). However, in ATD6-96 and ATD6-113 the M3 is
only partially covered by the ramus, the retromolar area is oblique,
the relief of the masseteric fossa is shallow, and the posterior
subalveolar fossa is moderately hollowed. In these mandibles, as
well as in ATD6-5 there is no alveolar prominence and the angle of
inclination of the mylohyoid groove is clearly lesser than 50
. In all
these features, the H. antecessor mandibles are derived in relation to
the earliest African Homo mandibles, as well as in relation to the
earliest Javanese H. erectus. Furthermore, the small height and
breadth of the H.antecessor mandibles contrast with the large di-
mensions of most African Homo specimens (except KNM-ER 1501
and OH 13), as well as with those of Sangiran 5, 8, 9, Hexian,
Tighenif 1, 2, and 3, Sidi Abderrahman, and Arago 13. Moreover, the
height of TD6 mandibles is lower than in the European Middle
Pleistocene hominins and the Neandertals (see Table 2 in Rosas and
Bermúdez de Castro, 1999). In this respect, H.antecessor is clearly
derived, sharing their gracility with most Chinese Middle Pleisto-
cene hominins (Carbonell et al., 2005). The mandible ATD6-96
exhibits a hypertrophied medial pterygoid tubercle (Carbonell
et al., 2005; Bermúdez de Castro et al., 2012), a feature that has
been included in the list of Neandertal apomorphies (Rak et al.,
1994; Weaver, 2009).
Concerning teeth, the H.antecessor permanent lower and upper
canines are derived regarding the Homo clade (see Martin
on-Torres
et al., 2008). However, they retain a vestigium of a cingulum and
present conspicuous essential ridges, unlike European Middle
Pleistocene hominins and H. neanderthalensis. The two H.ante-
cessor P
3
s (ATD6-7 and ATD6-69) show an incipient derived
morphology regarding the Homo clade. These teeth show a rela-
tively reduced lingual cusp and a nearly symmetric shape, although
not as pronounced as in the Middle and Late Pleistocene hominins
(G
omez-Robles et al., 2011). The P
4
in H.antecessor (ATD6-8, ATD6-
9, and ATD6-69) is more derived than the P
3
, similar to that of Asian
H.erectus,H.neanderthalensis and Atapuerca-SH hominins, but
primitive regarding H.sapiens. The buccal surface of upper pre-
molars show also a vestigium of a cingulum and several longitu-
dinal grooves that resemble that of other Early and Middle
Pleistocene fossils from Asia (except for Panxian Dadong, see Liu
et al., 2013) and Africa but not from Europe (Martin
on-Torres
et al., 2011; Xing et al., 2014, 2015). Both the crown and root of
the P
3
are remarkably primitive (Bermúdez de Castro et al., 1999;
G
omez-Robles et al., 2008) and different from the European Mid-
dle Pleistocene hominins, Neandertals and H.sapiens. Although the
H.antecessor P
4
s (ATD6-4 and ATD6-96) exhibit a primitive
morphology, with an elongated, subrectangular outline and a
mesially displaced metaconid, they also show a reduced occlusal
polygon. H.antecessor shares this feature with H.neanderthalensis
and the European Middle Pleistocene hominins (Martin
on-Torres
et al., 2006; see Table 4). The permanent upper first molars
(ATD6-18, ATD6-69, and ATD6-103) share their conformation with
Neandertals and some (but not all, e.g. Arago) European Middle
Pleistocene hominins (but see Martin
on-Torres et al., 2013 for dif-
ferences in cusp proportions). This morphology includes a rhom-
boidal and compressed occlusal polygon and a skewed external
outline with a bulging protrusion of the hypocone (G
omez-Robles
et al., 2007). The reduced occlusal polygon of the P
4
in H.ante-
cessor is another feature shared with H.neanderthalensis and the
European Middle Pleistocene hominins (Martin
on-Torres et al.,
2006). In addition, upper lateral incisors from TD6 display a trian-
gular shovel shape, with pronounced labial convexity (Martin
on-
Torres et al., 2007). This feature is part of the Eurasian dental
pattern (Martin
on-Torres et al., 2007) shared with Asian and Eu-
ropean Early and Middle Pleistocene hominins and Neandertals
(Table 4). Finally, and although the primitive M2 >M1 is the stan-
dard in both the maxillary and mandibular molar series, the strong
size reduction of the lower M3 is remarkable in the ATD6-96
mandible.
Lorenzo et al. (1999)'s conclusions about the study of the hand
and foot remains suggest that the TD6 hominins exhibit a
morphology more similar to modern humans than that of Nean-
dertals and their predecessors from the European Middle Pleisto-
cene. The long bones are fragmentary and their study (Carretero
et al., 1999; Pablos et al., 2012) yielded some interesting in-
dications about the phylogenetic position of the TD6 hominins
(Tables 2 and 4). Thus, the clavicle ATD6-50 is described by
Carretero et al. (1999) as “absolutely very long (maximum length),
relatively slender (low robusticity index) and with pronounced
shaft curvature and relatively small ephiphyses”, sharing its
morphology with Neandertals. Similarly, the humeri ATD6-121
(subadult) and ATD6-148 (adult) exhibit a large olecranon fossa
and very thin medial and lateral pillars, sharing these features with
European Middle Pleistocene hominins, Neandertals and, inter-
estingly, with the Bodo Middle Pleistocene humerus (Carretero
et al., 2009; Bermúdez de Castro et al., 2012). Finally, the talus
shows relatively narrower trochlea, a feature only shared with
Neandertals (Pablos et al., 2012).
5. Discussion
Although the number of specimens of the TD6 hypodigm is still
limited, there is enough information to offer proposals about the
hypothetical phylogenetic position of H.antecessor. We expect that
this information will be greatly increased in a near future, when we
excavate the majority of the TD6-2 level (about 80 square meters).
J.-M. Bermúdez-de-Castro et al. / Quaternary International xxx (2015) 1e10 5
Please cite this article in press as: Bermúdez-de-Castro, J.-M., et al., Homo antecessor: The state of the art eighteen years later, Quaternary
International (2015), http://dx.doi.org/10.1016/j.quaint.2015.03.049
The former hypothesis that H.antecessor could represent the last
common ancestor of H.neanderthalensis and H.sapiens (Bermúdez
de Castro et al., 1997) was formulated mainly due to the presence of
a modern-like face in the TD6 hypodigm. However, the geographic
position of the Iberian Peninsula in the westernmost extreme of the
Eurasian continent, as well as the geological age of the TD6 level
pose some difficulties to conciliate with the present paradigm
about the origin of our species. In fact, genetic data point to a more
recent divergence of modern humans and Neandertals (e.g. Noonan
et al., 2006; Endicott et al., 2010; Krause et al., 2010). The molecular
analyses made by Endicott et al. (2010) for the MCRA support the
hypothesis of a widely-dispersed ancestral species during the
middle part of the Middle Pleistocene, and a split that would have
occurred in a time range between 0.34 and 0.54 Ma, with a mean
age of 0.43 Ma. According to these authors, the split might have
coincided with the severe climate of MIS 12 (ca. 0.48e0.42 Ma).
Other results, however, suggest dates near to the MIS 21
(Ovchinnikov et al., 2002; Green et al., 2008; Langergraber et al.,
2012). Concerning the genetic approach there is no consensus
about the best method. Thus, recent analyses by Fu et al. (2013)
suggest a nuclear substitution rate that is approximately half that
of previous estimates based on fossil calibration. Therefore, and
according to these authors, major events in human evolution
occurred far earlier than previously thought. However, other spe-
cialists consider that the rate of mutation is slower than assumed so
far and thus, it would affect the hypothetic split of hominin lineages
(Hawks, 2012; Scally and Durbin, 2012). In consequence, it may be
recommendable to wait for an agreement before using genetics
arguments favouring or rejecting hypotheses on the split time of
Neandertals and modern humans.
Concerning the modern-like face of H.antecessor,Freidline et al.
(2013) proposed that evolution of modern-like facial morphology
occurred independently in Africa, Asia and Europe and several
times during the Early and the Middle Pleistocene. Freidline et al.
(2013)'s evolutionary interpretation of ATD6-69 is clearly influ-
enced by the most commonly accepted paradigm that the root of H.
sapiens lies in the African Middle Pleistocene populations (e.g.,
Stringer and Andrews, 1988). However, their interpretation has
been replied by Bermúdez de Castro and Martin
on-Torres (2014).
As we have previously explained (Bermúdez de Castro et al., 2003)
and we also defend in this review, we agree that Gran Dolina-TD6
hominins may not represent the origin of modern human pop-
ulations but a side branch restricted to Western Europe. However,
from a cladistic point of view this lineage would stem out very close
to the last common ancestor of H.sapiens and H.neanderthalensis.
On the other hand, we have showed that the hominins recov-
ered from the Sima del Elefante cave site (TE9 level), dated to about
1.1e1.2 Ma (Carbonell et al., 2008) and only 500 m far from Gran
Dolina, may represent a previous and different population dispersal
than that represented in TD6. Since the TE hominin sample is very
limited (Bermúdez de Castro et al., 2011; Martin
on-Torres et al.,
2011; Prado-Sim
on et al., 2011, 2012; Lorenzo et al., 2015) it is not
possible to draw sound conclusions from the anatomical compari-
sons with the TD6 hominins. However, differences in the inferred
behaviour and knapping strategies has led us to propose that the
TE9 and TD6 hominins can belong to two different migrations into
Western Europe (Bermúdez de Castro et al., 2013). Waiting for new
evidence, the TE9 hominins have been assigned to Homo sp.
(Bermúdez de Castro et al., 2011). In contrast to TE remains, the TD6
hominins exhibit enough information to posit phylogenetic hy-
potheses. They show a certain number of derived features, mainly
shared with Eurasian hominins and, in particular, with the Middle
Pleistocene and early Late Pleistocene populations. In this context,
it is surprising the relatively high number of features exclusively
shared with Neandertals and with the Atapuerca-SH hominins
(Table 4).
G
omez-Robles et al. (2013) have studied the dental morphology
of a large sample of hominins by combining 2D geometric mor-
phometrics method with the GLM method for estimating ancestral
traits (e.g. Martins and Hansen, 1997; Polly, 2008). These authors
concluded that no known fossil species is a suitable candidate for
being the last common ancestor of Neandertal and modern
humans. Thus, they exclude H.antecessor, but also other species like
H. heidelbergensis. Since all the European hominins posterior to 1.0
Ma exhibit “Neandertal features”they consider the possibility that
molecular estimates of the divergence between Neandertals and
modern humans may be underestimated. We agree with this
conclusion although, as we stated above, the time of divergence of
different lineages using genetic estimations ought to be considered
with caution. A second hypothesis suggested by G
omez-Robles
et al. (2013) points to the possibility that the divergence in dental
features between Neandertals and modern humans significantly
predates the complete speciation. This decoupled phenotypic dif-
ferentiation would have affected the dentition, but no other cranial
and postcranial features. However, we have confirmed that H.
antecessor shares some neurocranial, mandibular, and postcranial
features with the Atapuerca-SH hominins and the Neandertals
(Table 4). These features would be not Neandertal apomorphies,
but traits appeared in an ancestral and polymorphic population
during the Early Pleistocene (Bermúdez de Castro et al., 2012;
Bermúdez de Castro and Martin
on-Torres, 2013; Bermúdez de
Castro et al., 2014).
The TD6 hominins exhibit a suite of features lost in their African
ancestors and in the Dmanisi hominins (e.g. Martin
on-Torres et al.,
2008; Rightmire et al., 2008; Bermúdez de Castro et al., 2014).
Moreover, the dental features are in line with the Eurasian pattern
suggested by Martin
on-Torres et al. (2007). Although the TD6
hominins show a significant number of derived features shared
with Neandertals and modern humans, the hypothesis that H.
antecessor represent the last common ancestor of both hominin
lineages is not fully supported according to the dental morphology
(G
omez-Robles et al., 2013), or the geographic location of the Sierra
de Atapuerca. Nevertheless, all the evidences need to be reconciled
in a credible scenario. Bermúdez de Castro and Martin
on-Torres
(2013) have presented this scenario considering geographic and
climatic factors (see also Dennell et al., 2011; Martin
on-Torres et al.,
2011). Since it seems unlikely that Neandertal roots can stretch
back as deep as 1.0 Ma, we favour the existence of a Eurasian clade.
This clade would be the origin of some waves of populations into
Europe during the late Early Pleistocene and the Middle Pleisto-
cene. We also suggest that the settlement of Europe was compli-
cated by climatic and geographic factors, favouring isolation and
possible hybridation between paleodemes, including the first res-
idents. This scenario would explain the considerable diversity
observed in the European fossil record, evinced in the human
samples recovered from Ceprano, Arago, Sima de los Huesos or
Mala Balanica (e.g. Manzi., 2001; Roksandidic et al., 2011).
Since the most accepted theory in the present paradigm is that
modern humans originated in Africa and the lineage of Neandertals
developed in Europe, the physical and genetic divergence of the
two populations might have occurred either in Europe or in Africa.
The latter has been the preferred option of many colleagues,
perhaps because Africa has been traditionally considered as the
source of different migrations towards the Eurasian continent (e.g.
Stringer and Hublin, 1999; Hublin, 2009; Mounier et al., 2009;
Abbate and Sagri, 2011). In parallel with the current paradigm
concerning the origin of modern humans (Stringer and Andrews,
1988) it has also been suggested that the ancestors of
J.-M. Bermúdez-de-Castro et al. / Quaternary International xxx (2015) 1e106
Please cite this article in press as: Bermúdez-de-Castro, J.-M., et al., Homo antecessor: The state of the art eighteen years later, Quaternary
International (2015), http://dx.doi.org/10.1016/j.quaint.2015.03.049
Neandertals come from a significant out of Africa dispersal during
the Middle Pleistocene (Krause et al., 2010).
Nevertheless, and as we have stated in previous studies
(Martin
on-Torres, 2011; Bermúdez de Castro and Martin
on-Torres,
2013), Southwest Asia represents a suitable region for the evolution
of hominins during the entire Pleistocene (Hughes et al., 2007,
2008; Almogi-Labin, 2011). Furthermore, the Levantine Corridor
is a geographical crossroad between continents, and has been
identified as a true biodiversity hotspot (Carri
on et al., 2011). This
means that this region can be a source of phylogenetic diversity,
inducing speciation and reduced extinction rates (Kingston, 2007;
Spathelf and Waite, 2007; Ricklefs, 2010). Western Eurasia could
be then the homeland of an early hominin population, origin of
several migrations into Europe during the late Early and Middle
Pleistocene. Rightmire (1998) suggested that a speciation event
occurred in Africa during the very early Middle Pleistocene from
Homo erectus s.l. This author identified the speciation event with
the H.heidelbergensis species, and stated that it would be repre-
sented in both Africa (e.g., Bodo) and Europe (e.g., Petralona).
During the late Middle Pleistocene, either in Africa or Western
Eurasia, H.heidelbergensis species would have separated in would
have splitted into two branches, leading to the modern humans and
Neandertal lineages in Africa and Europe, respectively (Rightmire,
1998).
We agree with Rightmire (1998) in the general idea that there
was an early speciation process during the Pleistocene. However,
evidence from TD6 would push back in time this event. Also
interesting in this topic, is the inclusion of Western Eurasia in the
Rigtmire's scenario as the possible region for the splitting of
modern humans and Neandertals. In our view, the Western Eura-
sianeAfrican region could have been connected at least until the
so-called Middle Pleistocene Transition (MPT: 1.25e0.7 Ma)
throughout the Levantine Corridor, yielding support to the physical
and genetic continuity of this hypothetical AfricaneWestern Asian
population. This is a prerequisite for the splitting sometime of the
modern human and Neandertal lineages. According to new evi-
dences (e.g. Arnold, 2014; Arsuaga et al., 2014) and putting aside
the ongoing debates about the interpretation of the genetic data
(see above), this splitting might have occurred earlier than assumed
by Rightmire (1998). Furthermore, the Rightmire (1998)'s scenario
might be more complex, with the possible formation of different
Eurasian lineages during the Middle Pleistocene. Moreover and
regarding these questions, future comparative studies with African
late Early Pleistocene human fossils (Abbate et al., 1998; Manzi
et al., 2003; Macchiarelli et al., 2004; Zanolli et al., 2014) would
shed light to test this evolutionary scenario.
Concerning the geographic aspect of this scenario, it is very
interesting the O'Regan et al. (2011)'s review on the Afro-Eurasian
large-mammals dispersals during the Plio-Pleistocene. In their re-
view, these authors conclude that the majority of the large-
mammals migrations out of Africa occurred prior to 3.0 Ma or be-
tween 1.8 and 1.3 Ma. Later mammal movements out of Africa were
possibly sporadic. The faunal record of Western Europe from 1.2 Ma
onwards suggests transversal dispersals of large mammals origi-
nating in Asia (Cr
egut-Bonnoure, 1992 a,b; Kahlke, 1992; Kalkhe
et al., 2011, 2011; Carri
on et al., 2011; van der Made, 2011), obvi-
ously favoured by similar climatic conditions in Eurasia during the
late Early and Middle Pleistocene. O'Regan et al. (2011) also
conclude that a relatively small number of African Pleistocene taxa
emigrate into Eurasia, and viceversa. The suggestion made by Clarke
(2000) that the first Eurasian hominins could have moved back into
Africa is a very interesting idea, also considered by Manzi (2004),
Dennell and Roebroeks (2005),Rightmire et al., (2006),Martin
on-
Torres et al. (2007, 2008). These hypothetical population move-
ments in both directions through the Levantine Corridor may have
diminished or ceased due to the worsening climate occurred during
the MTP (see a detailed discussion in Bermúdez de Castro and
Martin
on-Torres, 2013 and references therein on geographical
and climatic aspects of the region). The climatic changes associated
to the MTP might be the main mechanism behind the physical
separation of the African/Western Eurasian population, previously
connected through the Levantine Corridor during the Early Pleis-
tocene. This separation would have preceded the genetic diver-
gence leading to modern humans and Neandertals.
6. Concluding remarks
H.antecessor exhibits a unique and very interesting mosaic of
primitive and derived features. A significant number of derived
features in this species points to a certain relationship with the
modern human and Neandertal lineages. In order to reconcile these
observations with the present fossil record, we suggest that H.
antecessor could represent one of the successive waves of pop-
ulations, which settled Europe during the Pleistocene and splitted
away from an early population probably living in Western Eurasia
or in Africa/Western Eurasia. This early population would be the
result of a cladogenetic event occurred during the late Early Pleis-
tocene. For this review, we prefer to avoid taxonomical questions
about this hypothetical population, and we are aware that some
colleagues may identify this cladogenetic event with H.erectus s.l.
Palaeogenetic studies ought to be refined in order to reduce the
time range for the physical and genetic divergence of the modern
humans and Neandertal lineages. However, we consider that this
event occurred during the evolution of this hypothetical popula-
tion. Independently from the name we could assign to the last
common ancestor of Neandertals and modern humans, and ac-
cording to the present evidence observed in the TD6 hominins,
both lineages would belong to the same clade of H.antecessor. The
recent genetic and morphological observations on the Atapuerca-
Sima de los Huesos hominins (Meyer et al., 2014; Arsuaga et al.,
2014) are very promising for understanding the evolutionary sce-
nario in Europe.
As a corollary of this report, we consider that the variability
observed in Asia (Anton, 2003; Vialet et al., 2010; Liu et al., 2013;
Xing et al., 2014, 2015) ought to be reconsidered. Independently
from taxonomical questions, the settlement of the Asian continent
might have occurred during the Early and Middle Pleistocene from
some successive migration population waves, some of them prob-
ably coming from Western Eurasia as well. Future comparative
studies between H.antecessor and other Middle Pleistocene Euro-
pean hominins with the Chinese fossil record could shed light on
these open questions.
Acknowledgements
The authors are grateful to all members of the Atapuerca
Research Team for their effort over decades recovering information
from the Sierra de Atapuerca sites and their superb research work.
We keep a special and grateful memory to Jaume Guiu whose
dedication and expert work in the TD6 excavation will be always
remembered. This article has been sponsored by the Direcci
on
General de Investigaci
on of the Spanish Ministry of Economía y
Competitividad, Grant numbers CGL2012- 38434-C03-02, the
Consejería de Cultura y Turismo and the Consejería de Familia e
Igualdad de Oportunidades of the Junta de Castilla y Le
on, the
Fundaci
on Atapuerca, and the Leakey Foundation through the
support of Gordon Getty and Dub Crook. Fig. 1 has been kindly
granted by Ana Isabel Ortega. The image processing was carried out
by Susana Sarmiento. Authors are also grateful to the reviewers,
who have contributed to improve the first manuscript.
J.-M. Bermúdez-de-Castro et al. / Quaternary International xxx (2015) 1e10 7
Please cite this article in press as: Bermúdez-de-Castro, J.-M., et al., Homo antecessor: The state of the art eighteen years later, Quaternary
International (2015), http://dx.doi.org/10.1016/j.quaint.2015.03.049
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