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Journal of Archaeological Science 40 (2013) 3532e3541

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Journal of Archaeological Science

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The Middle Stone Age human remains from Diepkloof Rock Shelter(Western Cape, South Africa)

Christine Verna a,*, Pierre-Jean Texier b, Jean-Philippe Rigaud b, Cedric Poggenpoel c,John Parkington c

aCNRS, UPR 2147, Dynamique de l’Évolution Humaine, 44 rue de l’Amiral Mouchez, 75014 Paris, Franceb PACEA, CNRS, Université de Bordeaux, UMR 5199, Avenue des Facultés, 33402 Talence, FrancecDepartment of Archaeology, University of Cape Town, Rondebosch, South Africa

a r t i c l e i n f o

Article history:Received 16 November 2012Received in revised form15 April 2013Accepted 16 April 2013

Keywords:Out of AfricaHomininsModern humansPleistoceneHowiesons PoortPhalangesTeeth

* Corresponding author. Tel.: þ33 143 135 611.E-mail addresses: christine.verna@evolhum.cnrs.fr

pacea.u-bordeaux1.fr (P.-J. Texier), John.Parkington@u

0305-4403/$ e see front matter � 2013 Elsevier Ltd.http://dx.doi.org/10.1016/j.jas.2013.04.011

a b s t r a c t

In the course of recent excavations at Diepkloof Rock Shelter (South Africa), three human remains werefound in the Middle Stone Age layers. These human remains are two pedal phalanges (intermediate anddistal) from a fifth ray, which belong to the same individual, and a deciduous first lower molar. The layersin which they were found represent the end of the Howiesons Poort and the beginning of post-Howiesons Poort occupation, and are radiometrically dated to MIS 3, between 45 and 65 kyr ago.They are thus very close in time to the assumed period of anatomically modern humans (AMH) dispersalout of Africa into Eurasia, a period for which very few remains are available in the African fossil record.Here, we describe these new remains and compare their morphology and dimensions to samples ofAfrican and Eurasian Pleistocene and Holocene humans. Our results show that the human remains fromDiepkloof Rock Shelter fall well within the range of variation of AMH. The phalanges are of very smallsize and indistinguishable from those of recent humans. In addition, our analysis of the dm1 underlines alarge size variation at the end of the MIS 4/beginning of the MIS 3 in the Western Cape. The discovery ofhuman remains at Diepkloof Rock Shelter, albeit limited to three small bones, enriches a poorly repre-sented chronological period of the African hominin fossil record.

� 2013 Elsevier Ltd. All rights reserved.

1. Introduction

In the last three decades, numerous fossil discoveries as wellas paleontological and genetic studies have led to a generalagreement that anatomically modern humans (AMH) emerged inAfrica 200 000e150 000 years ago (but see the recent discussionby Weaver, 2012). However, the pattern, mode and tempo ofAMH dispersal within and out of Africa are still unclear and arethe subject of lively discussions. Several morphological and ge-netic studies have recently suggested an ancient subdividedpopulation structure in Africa (Harpending et al., 1993; Harrisand Hey, 1999; Yu et al., 2002; Harding and McVean, 2004;Garrigan et al., 2005, 2007; Campbell and Tishkoff, 2008;Crevecoeur et al., 2009; Gunz et al., 2009a; Lambert and Tishkoff,2009; Henn et al., 2011b), and a complex scenario of migrations,extinctions and colonizations out-of and within the Africancontinent (Gunz et al., 2009a).

(C. Verna), pierrejean.texier@ct.ac.za (J. Parkington).

All rights reserved.

South Africa is a region of high interest when looking for theorigin of AMH dispersals. In the late 1970s, new developments in14C dating methods, as well as new excavations and reassessmentsof archeological sites, led to a drastic change in the understandingof South African MSA chronology (Rightmire, 1978, 1979; Bräuer,1984). This new chronological framework raised attention to theantiquity of AMH in sub-Saharan Africa and contributed to theemergence of the so-called Out-of-Africa model (Bräuer, 1984,1989; Stringer, 1989). Human remains found at the sites of BorderCave and Klasies River played an important role in these discus-sions (de Villiers, 1973; Rightmire, 1979, 1981, 1984; Klein, 1983;Bräuer, 1984; Corruccini, 1984; Wolpoff, 1989; Grün et al., 1990;Smith,1992; Groves and Lahr, 1994; Lahr and Foley,1994; Sillen andMorris, 1996; Grün and Beaumont, 2001). Furthermore, althoughmajor discoveries of fossils attributed to early AMH were made inEast Africa, particularly in the last decade (White et al., 2003), SouthAfrica has currently yielded one of the two largest samples of Af-rican Upper Pleistocene hominin remains preceding the Out-of-Africa event. The other important sample is a series of Moroccanfossils found in Aterian context (Hublin et al., 2012). In addition, thepresence in the South African Middle Stone Age (SA-MSA)

C. Verna et al. / Journal of Archaeological Science 40 (2013) 3532e3541 3533

archaeological record of several technological, social, economic andsymbolic changes and innovations has shed light on southwesternAfrica as the possible cradle of so-called behavioral modernity (seeMcBrearty and Brooks, 2000). This assertion was furthermoresupported in the last decade by the discovery in several SA-MSAsites containing bone tools (Henshilwood et al., 2001; Backwellet al., 2008) and symbolic elements such as engraved pieces ofochre (Henshilwood et al., 2002), shell beads (d’Errico et al., 2005;Henshilwood et al., 2009) as well as the numerous engraved ostricheggshells fragments found at Diepkloof Rock Shelter (Texier et al.,2010). Finally, genetic studies have shown that Khoisan-speakinghunteregatherers represent one of the oldest known lineages ofmodern humans (Gonder et al., 2007; Tishkoff et al., 2009;Veeramah et al., 2012). It has been recently suggested that AMHdispersal originated in southwestern Africa (Tishkoff et al., 2009;Henn et al., 2011b), although this proposal is controversial (Hennet al., 2011a; Hublin and Klein, 2011).

Currently, South Africa has yielded about a hundred bonesfound in at least 10 archaeological sites in MSA context, albeitmostly composed of fragments and isolated teeth. The largestknown sample comes from the site of Klasies River, which yieldedmore than 35 cranial, post-cranial and dental remains (Singer andWymer, 1982; Rightmire and Deacon, 1991, 2001) associatedmostly with MSA 2 and MSA 1 technocomplexes. The site of BorderCave yielded human remains in the 1940s and 1970s that includecranial and post-cranial remains as well as a child skeleton in as-sociation with MSA 1 and HP contexts, although the stratigraphiclocation of some of these remains is controversial (de Villiers, 1973;Grün et al., 1990, 2003; Sillen and Morris, 1996; Grün andBeaumont, 2001; Millard, 2006). More recently, the site of DieKelders Cave 1 yielded 24 isolated teeth, a mandibular fragmentand two hand phalanges in association with MSA 3 industries(Grine, 2000) whereas at the site of Blombos, nine isolated teethwere found in a Still Bay context (Grine and Henshilwood, 2002). Afew other isolated remains were found at the sites of Equus Cave(eight teeth and a mandible; Grine and Klein, 1985), Pinnacle Point(one cranial fragment and one tooth; Marean et al., 2004), SeaHarvest (one manual phalanx and one tooth; Grine and Klein,1993), Witkrans Cave (three teeth; McCrossin, 1992), Ysterfontein1 (three teeth; Klein, pers. com.), and possibly at Sibudu (two re-mains according to Plug, 2004). A few remains found at Hoedjies-punt were found in late Middle Pleistocene deposits but withoutdirect association with archaeological material (Stynder et al.,2001). Overall, all of these numerous but fragmentary remainscover a broad period of time ranging from the late Middle Pleis-tocene to the MIS 3 in the Upper Pleistocene, and thus documentonly partially the morphology and evolutionary history of the SA-MSA populations who occupied the region.

Interestingly, although SA-MSA fossil remains are often consid-ered as AMH, the debate regarding their “level of modernity” andtaxonomic attribution is still ongoing, with important implicationsregarding themode and tempo ofHomo sapiens evolutionary history(Smith, 1992; Pearson, 2000; Stringer, 2002; Bräuer, 2008; Tattersalland Schwartz, 2008; Rightmire, 2009). Several authors haveunderlined a mosaic-like morphology that combines derived fea-tures with the retention of primitive features, in particular in thepost-cranial skeleton (Churchill et al.,1996; Pearson andGrine,1996,1997; Pfeiffer and Zehr, 1996; Pearson, 2000; Rightmire et al., 2006;Bräuer, 2008). These observations raise questions regarding thedefinition of AMH and the interpretation of the Pleistocene Africanfossil record, as reflected by the occasional use of the term “near-modern” (Klein, 1999, 2008; Pearson, 2000; Rightmire, 2009). Someauthors favor the identification of several species (Tattersall andSchwartz, 2008) whereas others rather identify evolutionary“grades” within the species H. sapiens (Bräuer, 2008).

In this context, the discovery of human remains at DiepkloofRock Shelter (DRS) in association with MSA industries adds to theSA-MSA fossil record. These data are crucially needed to betterunderstand the evolutionary history of AMH. Here, we describethese remains, which were found in the uppermost part of theMiddle Stone Age sequence, at a chronological period close to theestimated time of dispersal of AMH in Eurasia.

2. The MSA human remains from DRS, archaeological contextand description

Diepkloof Rock Shelter (Western Cape, South Africa), exca-vated since 1998, is a MSA site that to date exposes a longarchaeological sequence of ca. 3.1 m deep. The site is locatedabout 180 km north of Cape Town and 14 km from the Atlanticcoast and the nearby site of Elands Bay Cave. Its stratigraphyextends from the OIS 5 until the beginning of the OIS 3 (Triboloet al., 2013) and notably includes the succession of the Still Bayand the Howiesons Poort (Porraz et al., 2013). The preservation ofthe archaeological remains is exceptional and, together with thehigh stratigraphic resolution (Miller et al., 2013) contributes torecognize Diepkloof Rock Shelter as a site-reference for the studyof the SA-MSA.

Three human remains, an isolated tooth and two phalanges,were found in the excavations of the southern sector (the Trench,see Parkington et al., 2013) in 2002 (Fig. 1). The tooth is a lower leftfirst deciduous molar that was unearthed in square F6 in a lenscalled Hearth below George. The two phalanges are an intermedi-ate and a distal pedal phalanges coming from the square C6, layerGavin. The remains are numbered DRS 1, 2 and 3. The stratigraphicunit (SU) George lies at the end of the Late Howiesons Poortoccupation of DRS, whereas Gavin belongs to the post-HP unit.These 2 SUs precisely mark the temporal limit observed in thedistribution of the Engraved ostrich eggshells (Texier et al., 2013):engravings are present in the SU George but none has been recor-ded in the overlying SU Gavin.

TL dating of the last period of the Howiesons Poort occupationfrom the northwestern sector of the excavations (complex OB1e4in the “back sector”) gave a mean age of 52 � 5 thousand years(ka) from four scattered estimates suffering from high environ-mental dose rate variability (Tribolo, 2003; Tribolo et al., 2013).The underlying unit is estimated 65 � 8 ka (complex OB5-end ofIntermediate HP) (Parkington et al., 2013; Tribolo et al., 2013). Inthe southern sector (the Trench) where the human remains werefound, OSL dates give consistent ages of between 58.1 � 1.9 and61.3 � 1.9 ka for this last HP occupation. The Layer George wasdated by OSL in the square C6 at 60.5 � 1.9 ka. In the same square,post-HP layers located above the layer Gavin gave ages of47.7 � 1.7 and 55.4 � 2.0 (Jacobs et al., 2008), consistent with aninfinite radiocarbon of >55 ka BP (Gif A 102381, wood fragmentfrom “Buddy-Becky”, square E6) (Tribolo, 2003). To summarize,the phalanges DRS 1 and DRS 2 were found associated with post-HP archaeological material and are dated to 46.0e57.4 ka, whereasthe lower deciduous molar DRS 1 is associated with the last HPoccupation of the site, which is dated around 60 ka.

2.1. DRS 1 and 2 e intermediate and distal pedal phalanges (Fig. 2)

These two phalanges articulate perfectly and belong with nodoubt to the same individual. They are very short, and this short-ness, in particular of the intermediate phalanx, suggests that theybelong to a fourth, or much more likely a fifth ray (see also below).The proximal epiphysis of the distal phalanx is fused to thediaphysis suggesting an age at death over 11 years based on data

Fig. 1. Map of the site showing the location of the human remains as well as the stratigraphic profile of the southern sector.

C. Verna et al. / Journal of Archaeological Science 40 (2013) 3532e35413534

known for recent humans (11e13 y for the females and 14e16 y forthe males; Scheuer and Black, 2000).

The distal phalanx is nearly complete, with a slight lateralerosion of the proximal epiphysis and of the plantar surface. Theintermediate phalanx preserves the complete distal head and partof the shaft. Its plantar surface is slightly more damaged proximallyand eroded. The head of the intermediate phalanx and the base ofthe distal one are well preserved and show no sign of pathologicalalteration.

The distal phalanx is short, its maximum length equals 7.1 mmand the mid-shaft breadth is 4.6 mm. The shaft is slightly asym-metric, and the rounded head shows only little enlargement of thedistal tuberosity. Its elliptical proximal articular surface is concavewith only a slight midline ridge, which is slightly more developedon its plantar half.

The intermediate phalanx, albeit incomplete, was also veryshort as shown by the preservation of a tiny part of the proximalarticular surface at 6.5 mm from the distal epiphysis. This shortnessalso supports the attribution of these phalanges to the fifth ray. Thedistal articular facet extends on both the plantar and dorsal faces ofthe shaft.

2.2. DRS 3 e first lower left deciduous molar (Fig. 3)

The crown of this molar is heavily worn and a small fragment ofenamel is lacking at its mesio-lingual corner (Fig. 2). Occlusalattrition has abraded all the topographic reliefs of the crown andthe occlusal surface is now a flat surface mostly composed bydentine. Only very small parts of the roots are present. Themorphology of their edge in apical view, in particular on the mesialside, suggests that the roots were resorbed on more than 3/4 oftheir length. This tooth might have then been lost ante-mortem. Ifhowever the toothwas still in situ, the age at death of the individualis estimated between 2 and 13 years based on known data for theage of the dm1 and P3 emergence on recent populations (Haavikko,1970; Gustafson and Koch, 1974; Liversidge and Molleson, 2004).The stage of root reabsorption however narrows this interval toprobably 9e10 y (Moorrees et al., 1963; Haavikko, 1973).

Morphologically, the crown is elongated and has a trapezoidaloutline in occlusal view, being wider bucco-lingually in its mesialpart. The buccal part of the crown is swollen mesio-lingually closeto the cervix, which corresponds to a strong tuberculum molare.Four well-developed cusps were present, but the presence of

Fig. 2. Intermediate and distal phalanges DRS 1 and 2 in dorsal view.

C. Verna et al. / Journal of Archaeological Science 40 (2013) 3532e3541 3535

additional small cusps cannot be assessed due to wear. The mesio-lingual cusp (metaconid) was more distally located than the mesio-buccal one (protoconid). These two mesial cusps were very close toeach other and were likely linked by a transverse crest that was

Fig. 3. The left dm1 DRS 3. Clockwise from top left: occlusal, buccal, distal and apicalviews.

probably continuous and not interrupted by a groove. However, thestage of wear prevents us to fully assess this morphology. Thepreserved morphology also shows that the mesial fossa was anoblique groove completely enclosed by the marginal mesial crest. Avery large central fossa, which is surrounded by an enamel ring,occupies a large part of the occlusal surface.

3. Comparative study e material and methods

Dimensions and indices of the remains from DRS are comparedto phalanges (rays 3e5) and dm1 of Pleistocene and Holocenehominins (see the Appendix for a detailed list of the sites andmodern collections included). Given the chronological age of theDRS human remains, reference is made primarily to lateMiddle andUpper Pleistocene human fossils from Africa and Eurasia. Thesefossils are attributed to Neandertals and anatomically modernhumans (AMH). The Neandertal sample encompasses specimensfound in Europe and Southwest Asia that belong to the marineisotope stages (MIS) 7e3. The AMH Pleistocene sample includesMIS 7e3 specimens divided in three sub-samples: South-Africanfossils found in MSA context (MSA), Middle Paleolithic specimensfrom the Near-East sites of Qafzeh and Skhul (MP) and Europeanfossils found in an Upper Paleolithic context (UP). In addition tothese Middle and Upper Pleistocene samples, our analyses alsoinclude a sample of North-African specimens from the TerminalPleistocene, which were found in association with Iberomaurusianindustries (IBM).

Pedal phalanges, in particular intermediate and distal, are veryrare in the fossil record and very few data are available in theliterature for Pleistocene AMH. Our comparisons with Early AMHare then limited the Qafzeh/Skhul specimens and two European UPspecimens: two Gravettian individuals from Dolní V�estonice(Sladek et al., 2000). An interesting comparison would includeNorth-African Pleistocene fossils associated with Mousterian orAterian technocomplexes. However, according to our knowledge,no pedal phalanges or dm1 have been reported from this archae-ological context. The only exception is the Irhoud 3 mandible, onwhich the dm1s are present but broken and do not allowcomparison.

Finally, metric data of Holocene recent humans (RH) are alsoincluded in our study. For dental metric analyses, the sample in-cludes specimens from historical periods from Europe and North-Africa. For the phalanges, we compare our sample to individualsfrom a Native American population as well as to a series of Frenchindividuals from the 20th century.

Morphometric comparative study of the distal phalanx in-cludes the following linear measurements: articular length (AL;M1); mid-diaphyseal height (MidH; M3); mid-diaphyseal breadth(MidB; M2); proximal maximum breadth (PrB; M2a) and height(PrH; M3a); distal maximum breadth (DiB; M2b) and height(DiH); proximal articular height (PrAH) and breadth (PrAB) (seeTrinkaus, 1975; Braüer, 1988 for the definition of the measure-ments). For the incomplete intermediate phalanx DRS 1, only themaximum distal length and breadth, as well as the distal articularbreadth (DiAB) can be measured and compared. In addition, fiveindices were computed using these measurements; they reflectthe proportions of proximal and distal articular surfaces, therelative distal and proximal breadth and the distal breadth vslength (see Table 1).

For the dm1, our metric comparison includes the maximummesio-distal (MD) and bucco-lingual (BL) diameters of the crown(M81 and M81e1, Braüer, 1988), as well as the crown index(BL � 100/MD) and overall crown area (BL � MD). Despite ratherstrong occlusal wear, both BL and MD can be accurately estimatedon DRS 3.

Table 1Univariate analyses of the dimensions of the intermediate (-IP) and distal (-DP) phalanges compared to Neandertals and Early AMH.

DRS Neand. [3e5] Neand. [4e5] MP [3e5] UP [3e5] MP þ UP [3e5]

n m sd Azs n m sd Azs n m sd n m sd n m sd Azs

DiH-IP 4.0 17 5.2 0.7 �0.8 8 5.4 0.9 �0.6 5 6.2 1.1 2 5.0 7 5.9 1.1 �0.7DiB-IP 6.4 5 9.7 0.6 L2.0 3 9.6 0.6 L1.2 2 10.6 2 8.0 4 9.3 1.7 �0.5DiAB-IP 6.3 16 9.8 1.0 L1.6 8 9.6 1.2 L1.2 5 9.6 1.0 2 8.0 7 9.1 1.1 L1.0AL-DP 6.6 10 11.4 1.2 L1.8 6 11.1 1.4 L1.3 4 8.9 1.3 4 8.5 1.6 8 8.7 1.4 �0.6MidB-DP 4.6 7 6.7 0.8 L1.0 3 6.1 0.6 �0.5 2 6.9 3 5.2 1.7 5 5.9 1.8 �0.3PrH-DP 4.7 12 8.4 1.2 L1.4 8 8.2 1.5 L1.0 2 7.3 4 5.3 1.0 6 6.0 1.3 �0.4PrB-DP 6.6 11 11.1 1.0 L1.9 7 10.9 0.9 L1.9 2 10.7 3 8.1 1.4 5 9.1 1.8 �0.5PrAH-DP 4.4 12 5.9 1.1 �0.6 8 5.8 1.2 �0.5 2 7.1 4 4.7 0.8 6 5.5 1.4 �0.3PrAB-DP 6.5 9 9.6 1.3 L1.0 5 9.6 1.4 �0.8 2 10.1 3 6.8 0.3 5 8.1 1.9 �0.3DiB-DP 4.7 10 9.4 1.5 L1.4 6 8.1 1.1 L1.2 2 7.1 3 5.6 0.6 5 6.2 1.0 �0.6DiH/DiAB-MP 63.5 16 54.5 7.3 0.58 9 57.5 7.4 0.3 5 64.5 2 62.6 7 64.0 5.4 0.0PrH/PrB-DP 72.0 11 74.2 10.1 �0.10 8 73.9 10.8 �0.1 2 68.5 3 67.0 6.9 5 67.6 5.1 0.3PrAH/PrAB-DP 68.8 9 57.9 8.3 0.57 6 58.1 9.2 0.5 2 66.3 3 71.8 9.0 5 69.6 7.1 0.0DiB/PrB-DP 71.7 9 79.0 13.4 �0.24 6 73.3 10.3 �0.1 2 67.0 2 65.9 4 66.4 5.1 0.3DiB/AL-DP 71.2 10 79.1 16.6 �0.21 7 73.6 12.3 �0.1 1 85.7 3 60.4 8.7 4 66.7 14.5 0.1

See text for the description of the measurements. Neand.: Neandertals; MP: Middle Paleolithic modern humans (Qafzeh/Skhul); UP: Upper Paleolithic modern humans; n:number of individuals;m: mean and sd: standard deviation of the sample. For each sample Azs is the adjusted z-score of the remains from DRS. All measurements in mm. Azsvalues that fall outside 95% of the variation of the reference population are highlighted in bold.

C. Verna et al. / Journal of Archaeological Science 40 (2013) 3532e35413536

The dimensions of the DRS phalanges and dm1 are compared toour Pleistocene and Holocene samples using univariate analyses,bivariate plots (providing 95% confidence ellipses of the referencegroups when enough specimens are present) and box plots(providing the median, minimumemaximum, and interquartileranges). Because of the small size of our fossil samples, we carriedout univariate analyses using the adjusted z-score (Azs) (Maureilleet al., 2001) in which 95% of the variation of the reference popu-lation is included between �1 and þ1. An Azs lower than �1 orhigher than þ1 is then outside 95% of the variation of the referencepopulation. For these univariate analyses and the box plots, eachindividual is represented by the mean of its right and left sideswhen available, whereas all right and left teeth are plotted on thebivariate graphs.

4. Comparative study e results

4.1. Comparative metrics of the phalanges

Overall, the phalanges from DRS are very small. All linear di-mensions but two (DiH of the IP and PrAH of the DP) are statisticallyexcluded from the Neandertal range of variation (Table 1). When

Table 2Univariate analyses of the dimensions of the intermediate (-IP) and distal (-DP) phalang

DRS IBM [3e5] IBM [4e5]

n m sd Azs n m sd

DiH-IP 4.0 42.0 5.2 0.6 L1.0 20 5.2 0.6DiB-IP 6.4 42 8.8 0.8 L1.5 20 8.8 0.6DiAB-IP 6.3 42.0 8.1 0.7 L1.3 20 8.0 0.8AL-DP 6.6 19.0 8.7 1.7 �0.6 9 7.6 0.8MidB-DP 4.6 20.0 6.6 1.1 �0.9 9 5.9 1.1PrH-DP 4.7 19.0 6.9 0.8 L1.3 9 6.5 0.8PrB-DP 6.6 19.0 10.1 1.0 L1.7 9 9.3 0.7PrAH-DP 4.4 19.0 5.8 0.7 �0.9 9 5.4 0.5PrAB-DP 6.5 19.0 8.9 0.9 L1.3 9 8.3 0.8DiB-DP 4.7 19.0 8.0 1.7 �0.9 9 6.7 1.0DiH/DiAB-MP 63.5 42.0 64.1 6.9 0.0 20 66.1 8.1PrH/PrB-DP 72.0 19.0 68.9 4.7 0.3 9 70.2 3.5PrAH/PrAB-DP 68.8 19.0 65.4 7.6 0.2 9 65.5 7.2DiB/PrB-DP 71.7 18.0 79.3 10.7 �0.3 9 72.0 8.1DiB/AL-DP 71.2 19.0 93.2 18.9 �0.6 9 88.4 14.6

See text for the description of the measurements. IBM: Iberomaurusians; RH-4 and RHindividuals; m: mean and sd: standard deviation of the sample. For each sample, Azs is

compared to phalanges from the rays 4 and 5 only, some of the DRSdimensions are then included in the Neandertal range of variation,but they remain low compared to the Neandertal sample and sixmeasurements are still statistically excluded from their range ofvariation (Table 1). The dimensions of the phalanges from DRS arealso lower than those of the Qafzeh and Skhul specimens and belowthe UP average (Table 1). When the MP and UP sub-samples arepooled together, univariate analyses show that the dimensions ofthe distal phalanx DRS 1 fall within their range of variation,whereas the articular breadth of the distal epiphysis (DiAB) of theintermediate phalanx DRS 2 is statistically excluded from the 95%variation (Table 1). All other dimensions arewithin the EAMH rangeof variation but below their average. The dimensions of the DRSphalanges are also rather low when compared to the Iber-omaurusian and Holocene sample (Table 2). The dimensions of theepiphyses of both phalanges are excluded or falls at the lower limitof the IBM range of variation, even if only the phalanges from therays 4 and 5 only are considered. When compared to the Holocenesamples, the epiphyseal dimensions of both phalanges as well asthe articular length and the proximal epiphysis dimensions of thedistal phalanx are excluded from the 4th ray range of variation.However, these dimensions fall well within the range of variation of

es compared to Iberomaurusians and recent humans.

RH-4 RH-5

Azs n m sd Azs n m sd Azs

�0.93 45 4.8 0.5 �0.8 15 4.8 0.7 �0.5L1.73 45 8.3 0.6 L1.6 14 7.5 0.8 �0.6L1.00 45 7.9 0.7 L1.1 13 6.8 0.6 �0.4�0.54 33 10.1 1.7 L1.0 36 8.7 1.7 �0.6�0.48 33 4.7 1.2 0.0 44 4.2 0.8 0.3�0.99 32 6.4 0.8 L1.0 37 5.9 0.6 L1.0L1.56 31 9.1 0.8 L1.5 39 8.7 0.9 L1.2�0.95 28 5.4 0.6 �0.8 34 5.2 0.5 �0.7L1.07 31 7.7 0.7 �0.9 33 7.1 0.8 �0.4�0.87 33 5.8 1.1 �0.5 45 5.1 1.0 �0.2�0.15 44 60.8 4.5 0.3 13 72 12.2 �0.30.23 29 70.5 5.2 0.1 37 67.3 5.9 0.50.20 26 72.0 9.2 �0.2 32 73.3 7.9 �0.3

�0.02 30 65.1 7.9 0.3 39 58.4 11.1 0.6�0.51 31 60.9 10.4 0.3 35 59.8 14.1 0.5

-5: recent humans, phalanges of the 4th and 5th rays respectively; n: number ofthe adjusted z-score of the remains from DRS. All measurements in mm.

Fig. 4. Dimensions of the phalanges DRS 1 and 2 compared to our comparative samples. a) Distal epiphysis dimensions of intermediate phalanges; b) overall dimensions of thedistal phalanges: mid-shaft breadth vs articular length; c) proximal articular dimensions of the distal phalanges breadth vs height; d) distal articular dimensions of the distalphalanges. N: Neandertals; MP: Middle Palaeolithic AMH; UP: Upper Palaeolithic AMH; RH-4 and RH-4: recent humans phalanges from the 4th and 5th rays. For the Pleistocenesamples, phalanges from the rays 3 to 5 are plotted but the 4th and 5th rays phalanges are indicated by the symbols IV and V respectively.

C. Verna et al. / Journal of Archaeological Science 40 (2013) 3532e3541 3537

the 5th ray phalanges, with the only exception of the proximalepiphysis breadth and height of the distal phalanx.

Fig. 4a shows that the distal articular surfaces of Neandertalintermediate phalanges are broader than UP, IBM and RH both inabsolute values and relative to their height. On this plot, DRS 1 fallsoutside the Neandertal range of variation, well below the di-mensions of the MP specimens as well as below the UP and IBMvalues. It plots at the lower limit of the recent human range ofvariation.

Fig. 4bed shows that, when compared to AMH, Neandertaldistal phalanges are long and wide, with wide proximal and distalepiphyses (see also Table 1). The distal epiphysis is especiallybroad, as shown by the indices DiB/PrB and DiB/AL (Tables 1 and 2and Fig. 4d). However, their range of variation overlaps largelywith the IBM sample. On these graphs, DRS 2 plots outside the

Neandertal range, quite far from the MP specimens, at the lowerlimit of the IBM range and within the recent human range. Onthese graphs, the phalanges from DRS and Dolní V�estonice arewell separated from the Neandertals by their dimensions andproportions and plot within the recent human range. The di-mensions of the distal phalanx of DRS are close to the 5th raydistal phalanx of Dolní V�estonice 16 and 3 (a gracile and smallindividual, Trinkaus and Jelinek, 1997).

4.2. Comparative metrics and morphology of the dm1

The crown of DRS 3 is overall small when compared to Nean-dertals and MP, but large when compared to RH as shown by itscrown area (Table 3). The value of this robustness index falls veryclose to the IBM and UP mean.

Fig. 5. Lower first deciduous molar mesio-distal and bucco-lingual crown dimensions for DRS 3 vs the comparative samples. AP6246 and AP6291: teeth from Die Kelders; N:Neandertals; MP: Middle Palaeolithic AMH; UP: Upper Palaeolithic AMH; RH: recent humans.

Table 3Univariate analyses of the dm1 dimensions.

DRS 3 Neand. MP UP IBM RH

n m sd Azs n m sd Azs n m sd Azs n m sd Azs n m sd Azs

MD 8.9 23 9.0 0.5 �0.05 5 9.1 0.2 �0.34 14 8.6 0.5 0.32 5 8.1 0.7 0.41 38 7.9 0.4 1.27BL 6.8 23 7.7 0.6 �0.72 6 7.5 0.5 �0.58 14 7.1 0.4 �0.28 6 7.5 0.3 �0.80 39 7.0 0.5 �0.12BL � 100/MD 76.4 23 85.3 3.7 L1.15 5 82.6 6.2 �0.36 14 82.9 4.4 �0.67 5 92.3 7.2 �0.80 38 88.2 7.2 �0.81BL � MD 60.9 23 69.0 8.6 �0.45 5 68.8 4.7 �0.61 14 60.7 6.6 0.01 5 60.2 7.1 0.04 38 54.5 5.5 0.57

Neand.: Neandertals; MP: Middle Paleolithic modern humans (Qafzeh/Skhul); UP: Upper Paleolithic modern humans; RH: recent humans; n: number of individuals;m: meanand sd: standard deviation of the sample. For each sample, Azs is the adjusted z-score of the remains from DRS. All measurements in mm. Azs values that fall outside 95% of thevariation of the reference population are highlighted in bold.

Fig. 6. Bivariate plot of the bucco-lingual vs mesio-distal crown diameters. DK-AP6246and AP6291: teeth from Die Kelders; N: Neandertals; MP: Middle Palaeolithic AMH;UP: Upper Palaeolithic AMH; RH: recent humans.

C. Verna et al. / Journal of Archaeological Science 40 (2013) 3532e35413538

The crown is elongated, with a rather low bucco-lingual crowndiameter (6.8 mm). This value is lower than most Neandertalsand all MP and IBM (Fig. 5). It falls in the lower half of the esti-mated range of variation of Neandertals, MP, UP and IBM(Table 3). This diameter is close to but below the average of ourrecent human sample. It also falls below the average of Bantu-speaking (n ¼ 35, m ¼ 7.1, sd ¼ 0.4) and San (n ¼ 97, m ¼ 6.9,sd ¼ 0.3) South-African groups measured by Grine (1984, 1986).In contrast, the mesio-distal diameter of the crown (8.9 mm) israther high, although it is slightly lower than the MP average. Itequals the Neandertal average, falls in the upper half of the UPand IBM range of variation and is statistically excluded from theRH range (Table 3). This diameter is also higher than the averageof the Bantu-speaking (n ¼ 35, m ¼ 8.2, sd ¼ 0.5) and San (n ¼ 90,m ¼ 8.1, sd ¼ 0.5) South-African groups measured by Grine (1984,1986). As a result, the crown index (76.4) is low and falls in thelower half of the MP, UP, IBM and RH ranges and is excluded fromthe Neandertal range. On the bivariate plot, DRS 3 falls outsidethe ellipse of our recent human sample (Fig. 6), far from the IBMindividuals and within the large overlap area of Neandertal andUP samples. It falls however at the limit of the Neandertal rangebecause of its low BL diameter. On this graph, DRS 3 plots close totwo UP specimens.

The crown of DRS 3 is also more elongated than two dm1 foundat Die Kelders (Grine, 2000). Its BL is very close to DK AP6291, but

C. Verna et al. / Journal of Archaeological Science 40 (2013) 3532e3541 3539

its MD is higher (8.9 mm vs 8.1 mm for AP6291), whereas bothdiameters are lower than on DK AP6246. The crown index of DRS(76.4) is thus much lower than the two Die Kelders ones (84.0 and86.8). Together, these three MSA dm1 represent a rather large rangeof size variation (see Figs. 4 and 5).

5. Discussion and conclusions

The site of DRS thus yielded two pedal phalanges (interme-diate and distal) from the fifth ray of a single individual in a post-HP MSA context, and a left dm1 attributed to the end of the LateHP occupation. Chronologically, these remains are very close intime to the assumed period of AMH dispersal out of Africa intoEurasia, a period for which very few remains are available in theAfrican fossil record. In particular, Upper Pleistocene fossils foundin East-Africa and attributed to AMH by several authors belong toolder chronological periods (e.g. Eyasi, Herto, Laetoli LH 18,Mumba, Mumbwa, Omo). This is also the case for almost all theUpper Pleistocene remains from South Africa, including KlasiesRiver (most of them associated with MSA 2 and MSA 1 in-dustries), Blombos (in a Still Bay context), and the specimensBorder Cave BC 1 and 2 (associated with MSA 1 industries; Grünand Beaumont, 2001; Millard, 2008). The few isolated remainsfound at Equus Cave, Sea Harvest and Witkrans were associatedwith MSA industries and certainly belong to the Upper Pleisto-cene, but lack precise dating (McCrossin, 1992; Klein, 2001;Millard, 2008). Overall, very few human remains are securelyassociated with the HP and post-HP technocomplexes. At KlasiesRiver, no human remains were found in the HP layer, and onlytwo parietal fragments are reported as coming from the MSA 3occupation of the site (Singer and Wymer, 1982). At Border Cave,despite uncertainties and controversy surrounding the prove-nance and antiquity of the remains, the mandible BC 5 is nowattributed to a HP layer dated to 66 kyr and the (now lost) infantskeleton BC 3 was also likely coming from a HP archaeologicalcontext (Millard, 2006, 2008). Finally, the largest series that isthe closest in time to the DRS human remains is the samplefound at Die Kelders. These remains were associated with a MSA3 technocomplex and date to sometime between ca. 59 and74 kyr (Grine et al., 2000). It is in this context of a drastic lack offossils at the HP/post-HP time period that the DRS remains takeon significance.

The phalanges of DRS are of very small size. By their di-mensions but also their proportions, and more specifically theproportions of the proximal epiphysis of the distal phalanx, theyare clearly distinct from Neandertals but also from the MiddlePleistocene AMH from Qafzeh and Skhul. They fall at the limit ofthe IBM range of variation but are close to some Upper Paleolithicspecimens. They are also well included in the range of variationof our recent human sample. The distal phalanx shows similarsize and proportions to the ray 5 phalanges of Dolní V�estonice,but we lack comparative material to assess the UP range ofvariation.

The crown of the deciduous molar DRS 3 is also overall smallwhen compared to Neandertal and MP humans, but rather largewhen compared to RH due to its large mesio-distal diameter. Thislarge mesio-distal diameter aligns it better with the Pleistocenehominins than with Holocene humans. The crown is stronglyelongated and its crown proportions and dimensions align it betterwith UP than with Neandertals, MP or IBM.

Thus, the human remains from DRS fit well into the variation ofUpper Pleistocene anatomically modern humans. The post-HPphalanges DRS 1 and DRS 2 are indistinguishable from those ofrecent humans. The crown dimensions of the HP first lower de-ciduous molar DRS 3 are not statistically incompatible with the

range of variation of recent humans. Its proportions align it betterwith Pleistocene AMH than with Holocene humans.

It is interesting to note that albeit very limited by the frag-mentary nature of the remains, our analyses underline differencesin morphology when the DRS specimens are compared to thechronologically older Middle Paleolithic AMH from Qafzeh andSkhul; the remains from DRS appear more similar to UP people interms of size and proportions of the pedal phalanges as well as theoverall shape of dm1. Other studies (Rightmire and Deacon, 1991;Rightmire et al., 2006) have shown morphological differences be-tween SA-MSA fossils and the Qafzeh/Skhul sample, and thisquestion certainly requires deeper investigations. However, too fewspecimens and too few anatomical features can however becompared, which prevents any relevant conclusion regarding thebiological affinities of the DRS specimens to other Upper Pleisto-cene samples.

Also interesting is the observation that the deciduous first molarDRS 3 has a more elongated crown than the two MSA specimensfrom Die Kelders (Grine, 2000). This isolated tooth thus adds to thevariation known for South-African MSA dm1 and taken all together,these three dm1 document a high size variability at the end of theMIS 4/beginning of the MIS 3 in the Western Cape region. Thisresult supports earlier observations underlining large size variationin the SA-MSA fossil record. In particular, large intra-site variabilityhas been discussed for themandibular and dental size at the sites ofKRM, Die Kelders and Blombos, which is usually interpreted asreflecting a high level of sexual dimorphism (Rightmire andDeacon, 1991, 2001; Lam et al., 1996; Grine et al., 2000; Grine andHenshilwood, 2002; Rightmire et al., 2006; Royer et al., 2009),although the presence of two distinct populations has also beensuggested to explain this pattern (Singer and Smith, 1969; Singerand Wymer, 1982).

Whether SA-MSA, East-Africa Middle Stone Age or North-AfricaAterian populations (if any of those) represent the population at theorigin of the AMH groups who colonized Eurasia is beyond thescope of this paper. The very fragmentary remains from DRS do notbring much more information to this debate for which new ana-lyses as well as new fossils are needed. However, the discovery ofhuman remains at DRS, albeit limited to three small bones, enrichesa poorly represented chronological period of the African homininfossil record.

Acknowledgments

The scientific project and excavation at Diepkloof have beenfunded by the French Ministry of Foreign Affairs (MAE), the Aqui-taine region, the Provence-Alpes-Côte-d’Azur region and by theCentre National de la Recherche Scientifique (CNRS). We are alsothankful to the Paleontological Scientific Trust (PAST) and the Na-tional Research Foundation (NRF) of South Africa for funding. TheUniversity of Cape Town has been of great support in providingspace, facilities and other logistical help. We are especially thankfulto Louisa Hutten and Dolores Jacobs. We are very grateful to E.Trinkaus and M. Toussaint who kindly allowed us to use theirmeasurements taken on Holocene samples. We also would like tothank Prof. H. de Lumley, A. Vialet and S. Renault (Institut de Palé-ontologie Humaine, Paris) for providing access and assistance to thestudy of the remains from IPH access to Qafzeh, Afalou and Taforaltcollections; A. Rosas for giving us access to the Holocene samplesstored in his Department; Ph. Mennecier, A. Fort and L. Huet forgiving us access to the Olivier’s collection at the Natural HistoryMuseum in Paris. We also thank S. Prat, T. Steele, C. Miller and threeanonymous reviewers for their useful comments and edits to thismanuscript.

C. Verna et al. / Journal of Archaeological Science 40 (2013) 3532e35413540

Appendix A. Comparative samples.

Geographicarea

Archaeological sites and collections Source of data

Lower dm1 Phalanges

Neandertals (MIS 7e3) Europe Amud, Archi, Châteauneuf, CombeGrenal, Devils’Tower, Engis*,La Ferrassie*, Pech-de-l’Azé*,Shanidar, Abri Suard*,Teshik-Tash [n ¼ 32]

Amud, La Ferrassie, Kiik-Koba, Krapina,Shanidar, Tabun [n ¼ 11]

Literature; *personal data; data fromE. Trinkaus (phalanges)

MP AMH (MIS 5) Middle-East Qafzeh and Skhul [n ¼ 8] Qafzeh and Skhul [n ¼ 5] Personal dataa (Qafzeh 6); Tillier, 1999;Vandermeersch, 1981

UP AMH (MIS 3) Europe Bacho Kiro, Grotte des Enfants*,Isturitz*, Lagar Velho, La Madeleine*,Quina-Aval*, Saint-Germain-la-Rivière [n ¼ 20]

Dolní V�estonice [n ¼ 2] Literature and *personal data

Ibero-Maurusian(Terminal Pleistocene)

North-Africa Afalou, Taforalt [n ¼ 13] Afalou, Taforalt [n ¼ 62] Personal dataa

Holocene humans Africa 5th century Nubian necropolis ofMirmad,c Egypt [n ¼ 6]

Personal data

Europe Medieval site of El Ejido Santaver,c Cuenca, Spain [n ¼ 11]

Olivier’s Collectionb [n ¼ 30] Personal data

Medieval site of Place Saint-Lambert,Liège, Belgium [n ¼ 19]

Data from M. Toussaint

800e1100 AD, Libben, Ohio [n ¼ 28] Data from E. Trinkaus

iencias Naturales in Madrid (Spain).

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