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Quaternary International 433 (2017) 22e31

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Quaternary International

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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, Spainb Institut Catal�a de paleoecologia Humana I Evoluci�o Social (IPHES), Marcel.li Domingo s/n, 43007, Tarragona, Spainc Laboratory of Human Evolution, Institute of Vertebrate Paleontology and Paleoanthropology (IVPP), Chines Academy of Sciences, 100044, Beijing, China

a r t i c l e i n f o

Article history:Available online 23 May 2015

Keywords:Human evolutionHomo antecessorSierra de AtapuercaGran Dolina

* Corresponding author.E-mail addresses: josemaria.bermudezdecastro@c

Castro), maria.martinon@cenieh.es (M. Martin�on-Torcenieh.es (L. Martín-Franc�es), mario.modesto@cenmarina.martinezdepinillos@cenieh.es (M. Martínezcenieh.es (C. García), valtes@iphes.cat (E. Carbonell).

http://dx.doi.org/10.1016/j.quaint.2015.03.0491040-6182/© 2015 Elsevier Ltd and INQUA. All rights

a b s t r a c t

It is eighteen years since the human fossils recovered from the TD6 level of the Gran Dolina cave site, inSierra 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. Theincrease of the African and Eurasian fossil record, as well as the application of new methodologicalapproaches, has led to competing interpretations about its hypothetical phylogenetic position andpossible evolutionary scenarios. At present, we can argue that this species is defined by a unique mosaicof primitive traits for the Homo clade, a certain number of derived features present in modern humans, asignificant suite of derived features shared with Neandertals and their ancestors in the European MiddlePleistocene (in particular with the Atapuerca-Sima de los Huesos hominins), and some derived featuresshared with the Chinese Middle Pleistocene hominins. From this evidence, we suggest that a speciationevent 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 regionof the Eurasian continent.

© 2015 Elsevier Ltd and INQUA. All rights reserved.

1. Introduction

During the 1994 and 1995 field seasons, an assemblage of nearninety human fossil remains and about 150 Mode 1 artifacts wererecovered 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 findingsoccurred during the excavation of an archaeological test pit of aboutsix square meters, made in order to evaluate the potential of thesite. The first paleomagnetic studies revealed the presence of theMatuyama/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,

enieh.es (J.-M. Bermúdez-de-res), laura.martinfrances@fa.ieh.es (M. Modesto-Mata),-de-Pinillos), cecilia.garcia@

reserved.

and we proposed a new Homo species, H. antecessor (Bermúdez deCastro 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 areanear the test pit made during the nineties of the twentieth century.During this excavation, the stratigraphic sequence of TD6 wasrefined (see Bermúdez de Castro et al., 2008a,b and Figs. 2 and 3)and new additional geochronological information is available fromthe Gran Dolina site (see below). Furthermore, new studies havebeen made from the TD6 human fossils. These studies, the findingof 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 Castroet al., 2011; Roksandic et al., 2011; Liu et al., 2013; Toro-Moyanoet al., 2013; Arsuaga et al., 2014; Xing et al., 2014, 2015) as well asthe reinterpretation of specimens recovered in the past (e.g. Manziet al., 2003; Mounier et al., 2009; Manzi et al., 2010; Stringer, 2012;Liu et al., 2013) have offered a considerable amount of informationto reconsider our first proposal and to look for alternative and

mailto:josemaria.bermudezdecastro@cenieh.esmailto:maria.martinon@cenieh.esmailto:laura.martinfrances@fa.cenieh.esmailto:laura.martinfrances@fa.cenieh.esmailto:mario.modesto@cenieh.esmailto:marina.martinezdepinillos@cenieh.esmailto:cecilia.garcia@cenieh.esmailto:cecilia.garcia@cenieh.esmailto:valtes@iphes.cathttp://crossmark.crossref.org/dialog/?doi=10.1016/j.quaint.2015.03.049&domain=pdfwww.sciencedirect.com/science/journal/10406182http://www.elsevier.com/locate/quainthttp://dx.doi.org/10.1016/j.quaint.2015.03.049http://dx.doi.org/10.1016/j.quaint.2015.03.049http://dx.doi.org/10.1016/j.quaint.2015.03.049

Fig. 1. The Gran Dolina cave site is about 27 m deep. The lower two thirds of thesequence belong to the Lower Pleistocene. A test pit made between 1993 and 1999, aswell as a vertical cut of the entire sequence allowed to found the human fossils fromthe TD6 level (see arrow and Fig. 2).

Fig. 2. Upper sequence of the lithostratigraphic unit TD6 from the Gran Dolina caveinfilling (Matuyama Chron), which includes the ‘‘Aurora archaeostratigraphic set’’(AAS), also known as TD6-2. All the human fossils of the H. antecessor hypodigm havebeen recovered from this section of the unit TD6. The AAS is not well defined as asequence of different layers on the test pit performed in the 1994e1996. Thus, the AAScorresponds 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 433 (2017) 22e31 23

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 resultspresented so far about the TD6 hypodigm, as well as the differentinterpretations made on the meaning of these hominins in thecontext of the African and Eurasian human evolution. It isimportant to note that a certain number of new analyses of theTD6 hominins are in progress, which undoubtedly will offeradditional information to test our hypothesis. Furthermore, in anear future the present Atapuerca Research Team will have ac-cess to a wide area of the different thin sublevels forming theAurora archaeostratigrafic set (also named TD6-2). This will be anopportunity to increase our knowledge of this hominin popula-tion, who lived in Western Europe during the late EarlyPleistocene.

2. The TD6 level

The Gran Dolina cave site (TD) fills up a large cavity about 27 mdeep andwith amaximumwidth of 17m (see Fig. 3 in Bermúdez deCastro et al., 2013). The stratigraphic section of the site was cut andexposed 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 isunder continuous refinement. There is a vertical cut of the sectionin progress, (e.g. Bermúdez de Castro et al., 2008a). In addition, weare currently studying a wide pit about 10 m deep excavated belowthe present level of the ancient railway (see Fig. 1). Par�es and P�erez-Gonz�alez (1995, 1999) observed a polarity reversal between TD7and T8, interpreted as the Matuyama/Brunhes boundary, meaningthat 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 fossilrecord of large- and micromammals, with a transition in TD6-2(Faunal Unit 4), TD7eTD8 (Faunal Unit 5) and drastic change inTD9eTD11 (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, whereasthe study of the amphibian and squamate reptile fossil record (Blainet al., 2009) of TD6-2 also suggests a slightly warmer temperaturethan today in Burgos.

The combination of paleomagnetic data and USeESR agessuggest a range between 0.78 and 0.86 Ma (million years ago) forTD6-2 (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 forTD6, which may correspond to MIS 25. The last systematicdating of the Gran Dolina sequence has been made by Moreno(2011) using the ESR dating method on optically bleachedquartz. This author analysed six samples for TD6 and TD7,obtaining an age range of 0.80e0.88 Ma for these levels, which isconsistent with the biostratigraphic and paleomagnetic analysesand suggest that the human assemblage was deposited duringMIS 21.

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.

J.-M. Bermúdez-de-Castro et al. / Quaternary International 433 (2017) 22e3124

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 eventsof cannibalism (Fern�andez-Jalvo et al., 1999; Carbonell et al., 2010).Nevertheless, we recorded and analyse a number of cranial andpostcranial features, mainly from the teeth, the mandibles and theface. Postcranial remains are also numerous and represent differentanatomical elements, including nearly twenty-five hand and footremains.

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 Arsuagaet al. (1999), Carretero et al. (1999), Lorenzo et al. (1999), Rosaset 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 havebeen 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).

Table 1List of the individuals represented in the TD6 hominin hypodigm.

Hominin Inventory number Specimen

H1 ATD6-1 Left lower CATD6-2 Left I2ATD6-3 Right P3ATD6-4 Right P4ATD6-5 Right mandible fragment with M1eATD6-6 Fragment of crown of right lower CATD6-7 Right P3

ATD6-8 Right P4

ATD6-9 Left P4

3.2. Minimum number of individuals (MNI)

In previous studies we assessed the possible minimum numberof individuals (MNI) currently represented in the TD6 hypodigm(e.g. Bermúdez de Castro et al., 2006). However, due to theconsiderable fragmentation of the hominin remains, this aspectremains difficult. Furthermore, the six sublevels (generally less than10 cm) identified during the last excavations (Bermúdez de Castroet al., 2008a,b) are condensed near the wall of the cave, where thetest pit was made during the nineties. Then, it was not possible tostate the precise provenance of each of the human remains found inthe test pit in correlation with the six levels, which were depositedin at least two different time events. Although we suspect that theMNI is higher than the estimation presented in Table 1, in this paperwe prefer to be conservative and to avoid speculations with theassociation of some isolated permanent and deciduous specimens.The present TD6 hypodigm includes four isolated deciduous teeth,two permanent Incisive germs and two permanent complete lowerincisors, some of which could represent additional immature oradult individuals. Summarizing, and considering that we haveexcavated only a small area of the TD6 level, our conclusions on theMNI are preliminary, except for the remarkable presence of a highpercentage of immature individuals in the TD6hypodigm (75%). Theage at death of the individuals presented in Table 1 is only anindicative approach. We have used modern human standards withthe aim of determining the MNI, but we are aware that this modelmay not apply for this Early Pleistocene population.

Age at deatha

13.5e14.5

M3 in-situ

Table 1 (continued )

Hominin Inventory number Specimen Age at deatha

ATD6-10 Right M1

ATD6-11 Left M1

ATD6-12 Right M2

H2 ATD6-14 Left maxillary fragment,with dcedm1 in-situ 3.5e4.0H3 ATD6-69 Maxilla and left zygomatic bone, including: left P3, M1, and unerupted M2, and right I2eM1 10.0e11.0H4 ATD6-125 Right P4 13.5e14.5H5 ATD6-94 Right M1 about 6.0

ATD6-103 Right M1

H6 ATD6-96 Left half mandible, including P3eM3 in-situ About 17.0H7 ATD6-113 Fragment of the left half of a mandible including M2 and M3 in-situ. About 17.0H8 ATD6-112 Right part of the mandibular corpus, from the symphysis to the crypt of the M2 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 433 (2017) 22e31 25

4. Results of the main studies performed in the TD6 humanfossils

In Tables 2, 3, and 4 we present the state (primitive or derived)of the main features identified so far in the TD6 hypodigm. Thestate of these features is evaluated in relation to the Homo clade.

Table 2Derived features shared by H. antecessor with modern humans.

� Face: e coronal orientation of the infraorbital surface, inferoposterior slope of this surface (with the canine fossa), anterior flexion in the maxillary surface andarcing of the zygomatico-alveolar crest, a projecting nose, and a zigomaxillary tubercle.

� Face: e modern (H. sapiens) growth remodelling pattern.� Skull: e convex superior border of the temporal squama.� Maxilla: e anterior position and almost vertical trajectory of the incisive canal.

Table 3Primitive features of H. antecessor regarding the Homo clade.

� Lower premolars: e complex 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 4Derived 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: e absolutely very long (maximum length), relatively slender (low robusticity index), pronounced shaft curvature, and relatively small ephiphyses.� Humerus: e large olecranon fossa and very thin medial and lateral pillars.� Talus: e relatively narrower trochlea (only shared with Neandertals).

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 ofthe midface of the immature specimen ATD6-69 (H3). These au-thors described this specimen as having a coronal orientation of theinfraorbital surface, an inferoposterior slope of this surface (withthe 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 nasalaperture. This last feature suggests that nose was projecting inATD6-69. 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 andH. sapiens regarding the facial growth remodeling pattern. Thispattern is totally different from the presumed primitive pattern ofthe Homo clade, observed in the specimen KNM-WT 15000.Another subadult specimen, ATD6-38, which is similar in size andshape to ATD6-69, also presents canine fossa (Arsuaga et al., 1999).Furthermore, the adult specimen ATD6-58, represented by a left

J.-M. Bermúdez-de-Castro et al. / Quaternary International 433 (2017) 22e3126

large zygomaxillary fragment, exhibits a remarkable canine fossa,as well as a great zygomaxillary tubercle placed in a maxillaryposition, that projects out about 3.3 mm (Arsuaga et al., 1999).Finally, an adult small zygomaxillary fragment (ATD6-19) alsoshows a zigomaxillary tubercle in the same position, which projectsout about 2.0 mm (Arsuaga et al., 1999). These authors suggest thatthe zigomaxillary tubercle may be present in the Zhoukoudianmaxilla II. Thus, the Zhoukoudian and the TD6 hominins wouldrepresent the unique presence of this facial feature prior to the LatePleistocene (Arsuaga et al., 1999). Furthermore, Vialet et al. (2010)have identified a facial pattern in the Chinese Middle Pleistocenespecimens, Yunxian II and Nankin 1, that is similar to that presentedby modern humans. Regarding all these results and since the Af-rican origin of our species seems to be undisputed for the majorityof paleoanthropologists, the presence of a modern-like human facein H. antecessor has been the subject of interest of some other re-searchers (e.g., Freidline et al., 2013). The latter made an interestingtheoretical ontogenetic study of the ATD6-69 face by means of 3Dgeometric morphometric analyses, with reference data mainlyfrom Neandertals and modern humans. Freidline et al. (2013)concluded that ATD6-69 exhibits a modern-like human midfacialmorphology, although their analyses placed ATD6-69 near themargin of modern human variation and intermediate between themodern humans and Middle Pleistocene human samples. Accord-ing to these authors, the face of this individual would not have beensignificantly altered in the course of the subsequent development.

Finally, and concerning the skull features, the TD6 homininsshare with Neandertals and modern humans a convex superiorborder of the temporal squama, as well as an anterior position ofthe incisive canal, which is nearly vertical (Arsuaga et al., 1999).These authors also concluded that the TD6 hominins show a smalland minimally projecting mastoid process and the anteriorlyobliterated digastric groove, a feature shared with Neandertals(Table 4).

Some of the mandibular features are primitive regarding theHomo clade (Table 3). However, in ATD6-96 and ATD6-113 theM3 isonly partially covered by the ramus, the retromolar area is oblique,the relief of the masseteric fossa is shallow, and the posteriorsubalveolar fossa is moderately hollowed. In these mandibles, aswell as in ATD6-5 there is no alveolar prominence and the angle ofinclination of the mylohyoid groove is clearly lesser than 50�. In allthese features, theH. antecessormandibles are derived in relation tothe earliest African Homo mandibles, as well as in relation to theearliest Javanese H. erectus. Furthermore, the small height andbreadth of the H. antecessor mandibles contrast with the large di-mensions of most African Homo specimens (except KNM-ER 1501and OH 13), as well as with those of Sangiran 5, 8, 9, Hexian,Tighenif 1, 2, and 3, Sidi Abderrahman, and Arago 13. Moreover, theheight of TD6 mandibles is lower than in the European MiddlePleistocene hominins and the Neandertals (see Table 2 in Rosas andBermúdez de Castro, 1999). In this respect, H. antecessor is clearlyderived, sharing their gracility with most Chinese Middle Pleisto-cene hominins (Carbonell et al., 2005). The mandible ATD6-96exhibits a hypertrophied medial pterygoid tubercle (Carbonellet al., 2005; Bermúdez de Castro et al., 2012), a feature that hasbeen included in the list of Neandertal apomorphies (Rak et al.,1994; Weaver, 2009).

Concerning teeth, the H. antecessor permanent lower and uppercanines are derived regarding the Homo clade (see Martin�on-Torreset al., 2008). However, they retain a vestigium of a cingulum andpresent conspicuous essential ridges, unlike European MiddlePleistocene hominins and H. neanderthalensis. The two H. ante-cessor P3s (ATD6-7 and ATD6-69) show an incipient derivedmorphology 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 P4 in H. antecessor (ATD6-8, ATD6-9, and ATD6-69) is more derived than the P3, similar to that of AsianH. erectus, H. neanderthalensis and Atapuerca-SH hominins, butprimitive 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 MiddlePleistocene fossils from Asia (except for Panxian Dadong, see Liuet al., 2013) and Africa but not from Europe (Martin�on-Torreset al., 2011; Xing et al., 2014, 2015). Both the crown and root ofthe P3 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 theH. antecessor P4s (ATD6-4 and ATD6-96) exhibit a primitivemorphology, with an elongated, subrectangular outline and amesially displaced metaconid, they also show a reduced occlusalpolygon. H. antecessor shares this feature with H. neanderthalensisand the European Middle Pleistocene hominins (Martin�on-Torreset al., 2006; see Table 4). The permanent upper first molars(ATD6-18, ATD6-69, and ATD6-103) share their conformation withNeandertals and some (but not all, e.g. Arago) European MiddlePleistocene 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 externaloutline with a bulging protrusion of the hypocone (G�omez-Robleset al., 2007). The reduced occlusal polygon of the P4 in H. ante-cessor is another feature shared with H. neanderthalensis and theEuropean 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 dentalpattern (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 strongsize reduction of the lower M3 is remarkable in the ATD6-96mandible.

Lorenzo et al. (1999)'s conclusions about the study of the handand foot remains suggest that the TD6 hominins exhibit amorphology 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 (Carreteroet 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 byCarretero et al. (1999) as “absolutely very long (maximum length),relatively slender (low robusticity index) and with pronouncedshaft curvature and relatively small ephiphyses”, sharing itsmorphology with Neandertals. Similarly, the humeri ATD6-121(subadult) and ATD6-148 (adult) exhibit a large olecranon fossaand very thin medial and lateral pillars, sharing these features withEuropean Middle Pleistocene hominins, Neandertals and, inter-estingly, with the Bodo Middle Pleistocene humerus (Carreteroet al., 2009; Bermúdez de Castro et al., 2012). Finally, the talusshows relatively narrower trochlea, a feature only shared withNeandertals (Pablos et al., 2012).

5. Discussion

Although the number of specimens of the TD6 hypodigm is stilllimited, there is enough information to offer proposals about thehypothetical phylogenetic position of H. antecessor. We expect thatthis informationwill be greatly increased in a near future, whenweexcavate the majority of the TD6-2 level (about 80 square meters).

J.-M. Bermúdez-de-Castro et al. / Quaternary International 433 (2017) 22e31 27

The former hypothesis thatH. antecessor could represent the lastcommon ancestor of H. neanderthalensis and H. sapiens (Bermúdezde Castro et al., 1997) was formulated mainly due to the presence ofa modern-like face in the TD6 hypodigm. However, the geographicposition of the Iberian Peninsula in thewesternmost extreme of theEurasian continent, as well as the geological age of the TD6 levelpose some difficulties to conciliate with the present paradigmabout the origin of our species. In fact, genetic data point to a morerecent divergence of modern humans and Neandertals (e.g. Noonanet al., 2006; Endicott et al., 2010; Krause et al., 2010). The molecularanalyses made by Endicott et al. (2010) for the MCRA support thehypothesis of a widely-dispersed ancestral species during themiddle part of the Middle Pleistocene, and a split that would haveoccurred in a time range between 0.34 and 0.54 Ma, with a meanage of 0.43 Ma. According to these authors, the split might havecoincided 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 consensusabout the best method. Thus, recent analyses by Fu et al. (2013)suggest a nuclear substitution rate that is approximately half thatof previous estimates based on fossil calibration. Therefore, andaccording to these authors, major events in human evolutionoccurred far earlier than previously thought. However, other spe-cialists consider that the rate of mutation is slower than assumed sofar and thus, it would affect the hypothetic split of hominin lineages(Hawks, 2012; Scally and Durbin, 2012). In consequence, it may berecommendable to wait for an agreement before using geneticsarguments favouring or rejecting hypotheses on the split time ofNeandertals and modern humans.

Concerning the modern-like face of H. antecessor, Freidline et al.(2013) proposed that evolution of modern-like facial morphologyoccurred independently in Africa, Asia and Europe and severaltimes 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 hasbeen 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-TD6hominins 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 lineagewould stem out very closeto 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 about1.1e1.2 Ma (Carbonell et al., 2008) and only 500 m far from GranDolina, may represent a previous and different population dispersalthan that represented in TD6. Since the TE hominin sample is verylimited (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 notpossible to draw sound conclusions from the anatomical compari-sons with the TD6 hominins. However, differences in the inferredbehaviour and knapping strategies has led us to propose that theTE9 and TD6 hominins can belong to two different migrations intoWestern Europe (Bermúdez de Castro et al., 2013). Waiting for newevidence, the TE9 hominins have been assigned to Homo sp.(Bermúdez de Castro et al., 2011). In contrast to TE remains, the TD6hominins exhibit enough information to posit phylogenetic hy-potheses. They show a certain number of derived features, mainlyshared with Eurasian hominins and, in particular, with the MiddlePleistocene 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 morphologyof a large sample of hominins by combining 2D geometric mor-phometrics method with the GLM method for estimating ancestraltraits (e.g. Martins and Hansen, 1997; Polly, 2008). These authorsconcluded that no known fossil species is a suitable candidate forbeing the last common ancestor of Neandertal and modernhumans. Thus, they excludeH. antecessor, but also other species likeH. heidelbergensis. Since all the European hominins posterior to 1.0Ma exhibit “Neandertal features” they consider the possibility thatmolecular estimates of the divergence between Neandertals andmodern humans may be underestimated. We agree with thisconclusion although, as we stated above, the time of divergence ofdifferent lineages using genetic estimations ought to be consideredwith caution. A second hypothesis suggested by G�omez-Robleset al. (2013) points to the possibility that the divergence in dentalfeatures between Neandertals and modern humans significantlypredates the complete speciation. This decoupled phenotypic dif-ferentiation would have affected the dentition, but no other cranialand postcranial features. However, we have confirmed that H.antecessor shares some neurocranial, mandibular, and postcranialfeatures 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 populationduring the Early Pleistocene (Bermúdez de Castro et al., 2012;Bermúdez de Castro and Martin�on-Torres, 2013; Bermúdez deCastro et al., 2014).

The TD6 hominins exhibit a suite of features lost in their Africanancestors 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 patternsuggested by Martin�on-Torres et al. (2007). Although the TD6hominins show a significant number of derived features sharedwith Neandertals and modern humans, the hypothesis that H.antecessor represent the last common ancestor of both homininlineages is not fully supported according to the dental morphology(G�omez-Robles et al., 2013), or the geographic location of the Sierrade Atapuerca. Nevertheless, all the evidences need to be reconciledin a credible scenario. Bermúdez de Castro and Martin�on-Torres(2013) have presented this scenario considering geographic andclimatic factors (see also Dennell et al., 2011; Martin�on-Torres et al.,2011). Since it seems unlikely that Neandertal roots can stretchback 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 intoEurope 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 andpossible hybridation between paleodemes, including the first res-idents. This scenario would explain the considerable diversityobserved in the European fossil record, evinced in the humansamples recovered from Ceprano, Arago, Sima de los Huesos orMala Balanica (e.g. Manzi., 2001; Roksandidic et al., 2011).

Since the most accepted theory in the present paradigm is thatmodern humans originated in Africa and the lineage of Neandertalsdeveloped in Europe, the physical and genetic divergence of thetwo 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 thesource 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 paradigmconcerning 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 433 (2017) 22e3128

Neandertals come from a significant out of Africa dispersal duringthe 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 evolutionof hominins during the entire Pleistocene (Hughes et al., 2007,2008; Almogi-Labin, 2011). Furthermore, the Levantine Corridoris a geographical crossroad between continents, and has beenidentified as a true biodiversity hotspot (Carri�on et al., 2011). Thismeans 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 couldbe then the homeland of an early hominin population, origin ofseveral migrations into Europe during the late Early and MiddlePleistocene. Rightmire (1998) suggested that a speciation eventoccurred in Africa during the very early Middle Pleistocene fromHomo erectus s.l. This author identified the speciation event withthe 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 WesternEurasia, H. heidelbergensis species would have separated in wouldhave splitted into two branches, leading to themodern humans andNeandertal lineages in Africa and Europe, respectively (Rightmire,1998).

We agree with Rightmire (1998) in the general idea that therewas an early speciation process during the Pleistocene. However,evidence from TD6 would push back in time this event. Alsointeresting in this topic, is the inclusion of Western Eurasia in theRigtmire's scenario as the possible region for the splitting ofmodern humans and Neandertals. In our view, the Western Eura-sianeAfrican region could have been connected at least until theso-called Middle Pleistocene Transition (MPT: 1.25e0.7 Ma)throughout the Levantine Corridor, yielding support to the physicaland genetic continuity of this hypothetical AfricaneWestern Asianpopulation. This is a prerequisite for the splitting sometime of themodern human and Neandertal lineages. According to new evi-dences (e.g. Arnold, 2014; Arsuaga et al., 2014) and putting asidethe ongoing debates about the interpretation of the genetic data(see above), this splittingmight have occurred earlier than assumedby Rightmire (1998). Furthermore, the Rightmire (1998)'s scenariomight be more complex, with the possible formation of differentEurasian lineages during the Middle Pleistocene. Moreover andregarding these questions, future comparative studies with Africanlate Early Pleistocene human fossils (Abbate et al., 1998; Manziet al., 2003; Macchiarelli et al., 2004; Zanolli et al., 2014) wouldshed light to test this evolutionary scenario.

Concerning the geographic aspect of this scenario, it is veryinteresting the O'Regan et al. (2011)'s review on the Afro-Eurasianlarge-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 werepossibly sporadic. The faunal record ofWestern Europe from 1.2 Maonwards suggests transversal dispersals of large mammals origi-nating in Asia (Cr�egut-Bonnoure, 1992 a,b; Kahlke, 1992; Kalkheet al., 2011, 2011; Carri�on et al., 2011; van der Made, 2011), obvi-ously favoured by similar climatic conditions in Eurasia during thelate Early and Middle Pleistocene. O'Regan et al. (2011) alsoconclude that a relatively small number of African Pleistocene taxaemigrate into Eurasia, and viceversa. The suggestionmade by Clarke(2000) that the first Eurasian hominins could havemoved back intoAfrica 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 theworsening climate occurred duringthe MTP (see a detailed discussion in Bermúdez de Castro andMartin�on-Torres, 2013 and references therein on geographicaland climatic aspects of the region). The climatic changes associatedto the MTP might be the main mechanism behind the physicalseparation of the African/Western Eurasian population, previouslyconnected 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 ofprimitive and derived features. A significant number of derivedfeatures in this species points to a certain relationship with themodern human and Neandertal lineages. In order to reconcile theseobservations 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 splittedaway from an early population probably living in Western Eurasiaor in Africa/Western Eurasia. This early population would be theresult of a cladogenetic event occurred during the late Early Pleis-tocene. For this review, we prefer to avoid taxonomical questionsabout this hypothetical population, and we are aware that somecolleagues may identify this cladogenetic event with H. erectus s.l.

Palaeogenetic studies ought to be refined in order to reduce thetime range for the physical and genetic divergence of the modernhumans and Neandertal lineages. However, we consider that thisevent occurred during the evolution of this hypothetical popula-tion. Independently from the name we could assign to the lastcommon 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. Therecent 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 variabilityobserved in Asia (Anton, 2003; Vialet et al., 2010; Liu et al., 2013;Xing et al., 2014, 2015) ought to be reconsidered. Independentlyfrom taxonomical questions, the settlement of the Asian continentmight have occurred during the Early and Middle Pleistocene fromsome successive migration population waves, some of them prob-ably coming from Western Eurasia as well. Future comparativestudies between H. antecessor and other Middle Pleistocene Euro-pean hominins with the Chinese fossil record could shed light onthese open questions.

Acknowledgements

The authors are grateful to all members of the AtapuercaResearch Team for their effort over decades recovering informationfrom the Sierra de Atapuerca sites and their superb research work.We keep a special and grateful memory to Jaume Guiu whosededication and expert work in the TD6 excavation will be alwaysremembered. This article has been sponsored by the Direcci�onGeneral de Investigaci�on of the Spanish Ministry of Economía yCompetitividad, Grant numbers CGL2012- 38434-C03-02, theConsejería de Cultura y Turismo and the Consejería de Familia eIgualdad de Oportunidades of the Junta de Castilla y Le�on, theFundaci�on Atapuerca, and the Leakey Foundation through thesupport of Gordon Getty and Dub Crook. Fig. 1 has been kindlygranted by Ana Isabel Ortega. The image processing was carried outby 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 433 (2017) 22e31 29

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