Modern human cranial diversity in the Late ... - Wiley Online Library

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 140:347–358 (2009)

Modern Human Cranial Diversity in the Late Pleistocene of Africa and Eurasia: Evidence From Nazlet Khater, Pes tera cu Oase, and Hofmeyr Isabelle Crevecoeur,1,2* He´le`ne Rougier,1,2,3 Frederick Grine,4,5 and Alain Froment6 1

Laboratoire d’Anthropologie et de Pre´histoire, Institut royal des Sciences naturelles de Belgique (IRSNB), 1000 Bruxelles, Belgique 2 UMR 5199 - PACEA, Laboratoire d’Anthropologie des Populations du Passe´, Universite´ Bordeaux 1, 33405 Talence, France 3 Department of Anthropology, California State University Northridge, Northridge, CA 91330 4 Department of Anthropology, Stony Brook University, Stony Brook, NY 11794-4364 5 Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY 11794-4364 6 De´partement d’Anthropologie, Museé de l’Homme, 75116 Paris, France KEY WORDS

modern human origins; Africa; Eurasia; craniometric data

ABSTRACT The origin and evolutionary history of modern humans is of considerable interest to paleoanthropologists and geneticists alike. Paleontological evidence suggests that recent humans originated and expanded from an African lineage that may have undergone demographic crises in the Late Pleistocene according to archaeological and genetic data. This would suggest that extant human populations derive from, and perhaps sample a restricted part of the genetic and morphological variation that was present in the Late Pleistocene. Crania that date to Marine Isotope Stage 3 should yield information pertaining to the level of Late Pleistocene human phenotypic diversity and its evolution in modern humans. The Nazlet Khater (NK) and Hofmeyr (HOF) crania from Egypt and South Africa, together with penecontemporane-

ous specimens from the Pes tera cu Oase in Romania, permit preliminary assessment of variation among modern humans from geographically disparate regions at this time. Morphometric and morphological comparisons with other Late Pleistocene modern human specimens, and with 23 recent human population samples, reveal that elevated levels of variation are present throughout the Late Pleistocene. Comparison of Holocene and Late Pleistocene craniometric variation through resampling analyses supports hypotheses derived from genetic data suggesting that present phenotypic variation may represent only a restricted part of Late Pleistocene human diversity. The Nazlet Khater, Hofmeyr, and Oase specimens provide a unique glimpse of that diversity. Am J Phys Anthropol 140:347–358, 2009. V 2009 Wiley-Liss, Inc.

Two episodes that relate to the origin and diversity of anatomically modern humans have been the subject of intense investigation. The first concerns their emergence in Africa and subsequent appearance in southwest Asia during marine isotope stages (MIS) 6 and 5 (190–70 ka) (Vandermeersch, 1981; Day and Stringer, 1982; McDermott et al., 1993; Clark et al., 2003; White et al., 2003; Haile-Selassie et al., 2004; McDougall et al., 2005). The earlier dates for the African fossils, together with copious genetic data point to an African origin for modern humans (e.g., Garrigan and Hammer, 2006; Liu et al., 2006; Fagundes et al., 2007; Gonder et al., 2007; Handley et al., 2007; Underhill and Kivisild, 2007; Behar et al., 2008; Li et al., 2008). These fossils are characterized by a mixture of archaic and modern morphological features (Vandermeersch, 1981; Day and Stringer, 1982; White et al., 2003). The second period that has been studied intensively relates to MIS 2 and 1 (\25 ka). A number of well-dated and complete specimens that derive from this temporal period have been discovered in many parts of the world, enabling researchers to focus on the characterization of recent human variability (e.g., Lahr, 1996; Demeter et al., 2003). Genetic studies suggest a recent origin from an ‘‘African genetic stock’’ that underwent one or more demographic crises followed by waves of expansion (Excoffier, 2002; Marth et al., 2003; Garrigan and Hammer, 2006; Field et al., 2007; Manica et al., 2007; Lohmueller et al., 2008).

This could imply that extant human populations derive from a restricted part of past human variation. Archaeological and genetic evidence appear to identify a major population collapse and recovery at the end of MIS 4, at some 60–50 ka (Mellars, 2006a; Field et al., 2007; Manica et al., 2007). It has been surmised that the first wave of dispersal out of Africa may have taken

C 2009 V

WILEY-LISS, INC.

C

Grant sponsor: NSF; Grant number: BCS-0409194; Grant sponsor: the Wenner-Gren Foundation; Grant number: 7111; Grant sponsor: the Romanian National Council for Academic Research; Grant number: CNCSIS 1258/2005; Grant sponsors: Washington University, the Leakey Foundation, the Centro Nacional de Arqueologia Naútica e Subaqua´tica (Instituto Portugueˆs de Arqueologia), the Royal Belgian Institute of Natural Sciences, the Fondation Fyssen, the Leakey Foundation, the Wenner-Gren Foundation, National Geographic, the American Philosophical Society, Stony Brook University. *Correspondence to: Isabelle Crevecoeur, Laboratoire d’Anthropologie et de Pre´histoire, Institut royal des Sciences naturelles de Belgique (IRSNB), 29 rue Vautier, 1000 Bruxelles, Belgique. E-mail: [email protected] Received 29 July 2008; accepted 3 March 2009 DOI 10.1002/ajpa.21080 Published online 7 May 2009 in Wiley InterScience (www.interscience.wiley.com).

348

I. CREVECOEUR ET AL.

Fig. 1. Lateral view of the skulls of Hofmeyr (image flipped), Oase 2, and Nazlet Khater 2 (from left to right). [Color figure can be viewed in the online issue, which is available at www.interscience. wiley.com.]

Fig. 2. Lateral view of Oase 1 and NK 2 mandibles (from left to right). [Color figure can be viewed in the online issue, which is available at www. interscience.wiley.com.]

place at this time (Field and Lahr, 2005), although various genetic studies have placed this anywhere between 70 and 25 ka (e.g., Quintana-Murci et al., 1999; Ingman et al., 2000; Underhill et al., 2000; Macaulay et al., 2005; Takasaka et al., 2006; Fagundes et al., 2007). The middle of this range (ca. 45–35 ka) corresponds not only with the appearance of Late Stone Age (LSA) industries in sub-Saharan Africa (Ambrose, 1998) but also with the earliest Upper Paleolithic (UP) industries and modern human skeletons in Eurasia (Mellars, 2006b). Whatever the number or exact age(s) of this (these) bottleneck(s), the genetic evidence underscores the significance of Late Pleistocene human morphology, inasmuch as specimens that date to MIS 4 and 3 should yield information pertaining to diversity prior to the bottleneck(s). Indeed, several craniometric studies have emphasized greater variation among some Late Pleistocene African and Eurasian specimens than is evinced by recent human populations (e.g., Corruccini, 1992; Kidder et al., 1992; Braüer and Singer, 1996). Unfortunately, human remains from Africa that date to between ca. 65 and 25 ka are virtually unknown. The skeleton of Nazlet Khater 2 (NK 2) from Egypt and the Hofmeyr (HOF) cranium from South Africa are the only two reasonably complete and well-dated African specimens from this interval. Both present a suite of features that clearly align them with modern humans. The NK 2 skeleton has been directly dated by ESR on tooth enamel fragments to 38 6 6 ka (Gru¨n, personal communicaAmerican Journal of Physical Anthropology

tion1), and its skull and mandible exhibit several archaic features (Thoma, 1984; Crevecoeur and Trinkaus, 2004; Crevecoeur, 2008). The skull from Hofmeyr, which has been dated to 36.2 6 3.3 ka by a combination of optically stimulated luminescence and uranium-series methods, is anatomically modern, but also displays some archaic features (Grine et al., 2007). Of similar antiquity, the Pes tera cu Oase specimens from Romania have been dated to 40,440 6 1,030 calendar years BP (34,950, 1990, 2890 14C BP) (Trinkaus et al., 2003; Rougier et al., 2007). These consist of a complete mandible (Oase 1; OAS 1) and a nearly complete cranium (Oase 2; OAS 2), and are among the oldest securely dated anatomically modern human fossils from Eurasia (Barker et al., 2007; Shang et al., 2007). The Nazlet Khater, Oase and Hofmeyr specimens (Figs. 1 and 2) provide a tantalizing glimpse of African and Eurasian human cranial diversity during MIS 3. We here report on a study of these fossils, comparing them with other Pleistocene specimens, and a reference sample of 2,171 crania representing a worldwide distribution of 23 recent human populations. This study entailed examination of a number of morphological features and uni- and multivariate analyses of metrical variables of the cranium and mandible. The goals of this study are to document the morphometric characteristics of these three important Late Pleistocene specimens, and to compare their variation to that exhibited by earlier and later crania from Africa and Eurasia. Through the use of bootstrapping tech-

LATE PLEISTOCENE HUMAN CRANIAL DIVERSITY TABLE 1. Extant human populations sampled for the bootstrap analyses Extant human populations Algerian Alishar Huÿu¨k (Iron Age) Atayal Australian Aborigines Baye’s caves (Chalcolithic) Bedouin Buriat Khoe-San French Fernan-Vaz Hainan Inuit Moriori Norse (Medieval) Nubia (Meroitic) Peruvian Pygmies Santa Cruz Island South Japan Tepe Hissar (Chalcolithic) Tetela Tolai Zalavar Total

N 63 22 47 100 116 32 110 170 250 109 83 108 107 110 51 110 16 102 91 116 50 110 98 2,171

Location Maghreb (North Africa) Turkey (Eurasia) Taiwan (South Asia) Australia France (West Europe) North Africa and South-West Asia Siberia (North Asia) South Africa (South Africa) France (West Europe) Gabon (West Africa) China (South Asia) Arctic New Zealand (Australia) Norway (North Europe) Nubia (North Africa) Peru (South America) Central Africa U.S.A. (North America) Japan (East Asia) Iran (South-West Asia) D.R.C. (Central Africa) Papua New Guinea (South-East Asia) Hungary (East Europe)

The number of individuals constituting each group (N) and their geographical provenience are indicated. Cranial measurements were compiled from the literature (Shrubsall, 1898; CrewdsonBenington, 1911; Krogman and Schmidt, 1933; Matiegka and Maly, 1938; Riquet, 1953; Milicer-Gruzewska, 1955; Demoulin, 1972; Marquer, 1972; Buyle-Bodin and Philippe, 1982; Howells, 1989; Ribot, 1998) by A.F.

niques, we estimate the probability that three crania displaying the level of variation exhibited by the NK 2, HOF, and OAS 2 specimens could be sampled at random within recent or other fossil samples.

MATERIALS AND METHODS Comparative samples The recent human sample includes 2,171 individuals from 23 geographically disparate populations. Five of these date from Chalcolithic to Medieval periods (Table 1). These morphometric data were extracted from published sources by A.F. We also consider several samples representing different prehistoric periods (Table 2). The first sample consists of late Middle to early Late Pleistocene Homo sapiens (MPHS). Following other workers (e.g., Day et al., 1980; Lieberman et al., 2002; White et al., 2003), this sample comprises the Qafzeh and Skhul specimens, as well as Aduma (ADU-VP-1/3), Bouri (BOU-VP-5/1), Omo-Kibish 1 and 2, Herto (BOU-VP-16/1), Jebel Irhoud 1 and 2, Ngaloba (LH18), and the Aterian specimens of Te´mara and Dar-es-Soltan 5. The second fossil sample consists of Early and Late Upper Paleolithic specimens from Europe (EUP) and includes specimens from Mladecˇ, Muierii, and Cioclovina, which are geographically proximate to OAS, but slightly younger.

349

The third fossil group includes the Afalou and Taforalt series (LUPAW) and the Jebel Sahaba and Wadi Kubbaniya specimens (LUPAE) from North Africa. The Ohalo H2 and Wadi Mataha F-81 specimens are included in this sample in view of their chronological and geographical proximity. The final comparative sample is composed of Neandertal (NEAND) crania, and is included to document variability in another Pleistocene hominin group.

Statistical analyses The measurements employed in the analyses are as defined by Howells (1973) and Martin (Braüer, 1988). Principal component analyses (PCAs) were performed with STATlab (STATlab, 1991). Each variable was first tested for normality, and a correlation matrix was then used (analysis in R-mode; Middleton, 2000) to identify highly correlated variables (i.e., those responsible for redundant information), and those that contributed minimally to the formation of the major principal components (PCs). This selection process resulted in from six to eight variables being used in the PCA in Q-mode (Middleton, 2000) for the Pleistocene samples. Raw as well as size-adjusted data were used for the PCAs. Size-adjusted variables were computed following Darroch and Mosimann (1985) to define shape. As demonstrated by Jungers et al. (1995), this method may identify differently sized individuals with the same shape. The squared Mahalanobis distances used in the resampling procedures derive from the discriminant analysis of eight size-adjusted craniofacial dimensions. Each individual was characterized by its distance from the centroid of the recent human sample. To assess the probability (P-value) of finding three recent crania that exhibit the same sum of distances as NK 2, OAS 2, and HOF, we performed a random resampling procedure with replacement. We repeatedly (10,000 times) drew a sample of three individuals from the extant human populations and computed the sum of their squared Mahalanobis distances to obtain a distribution range of expected sums. The same procedure was applied to the African and European samples that date to MIS 3–2 (EUP and LUPA). The two dispersions were tested for normality by the Shapiro-Wilk test, and the variance of the two groups was evaluated for equivalence using the F-Snedecor method.

RESULTS Morphological variation Table 3 lists morphological features exhibited by NK 2, OAS 1, OAS 2, and HOF. Those traits that are defined as being ‘‘archaic’’ are shared with Early and Middle Pleistocene Homo to the exclusion of anatomically modern humans. We have differentiated between archaic features that are manifestly associated with the masticatory apparatus, and those that may be independent of it. Following Friess (1999) and Lieberman et al. (2002), we consider the traits that are likely related to mastication as a single, complex feature. The low position of maximum cranial breadth in NK 2 may be an archaic feature (Dean et al., 1998), insofar as it is present in African and Asian archaic Homo (Grimaud, 1982), although this occurs quite frequently American Journal of Physical Anthropology

350


TABLE 2. Definition of the comparative groups with the list of every specimen included and the total number of individuals (N) Fossil samples

Individuals

N

MPHS: Late Middle to Early Upper Pleistocene African and Eurasian specimens Africa Aduma (ADU-VP-1/3); Bouri (BOU-VP-5/1); Dar-es-Soltan 5; Herto (BOU-VP-16/1); Jebel Irhoud 1 and 2; Ngaloba H18; Omo Kibish 1 and 2; Temara. Southwest Asia Qafzeh (3, 5, 6, 7, and 9) and Skhul (2, 4, 5, 6, and 9)

18

EUP: European Early and Middle Upper Paleolithic modern humans Abri Pataud 1; Arene Candide 1; Barma Grande (1 and 2); Brno 2; Caviglione 1; Cioclovina 1; Cro Magnon (1, 2, and 3); Dolnı´ Veˇstonice (1, 2, 3, 11, 13, 14, 15, and 16); Grotte des Enfants (4, 5, and 6); Mladecˇ (1, 2, 5, 6, and 8); Muierii 1; Paglicci 25; Pavlov 1; Predmostı` (1, 3, 4, 5, 9, and 10); and Sunghir (1 and 5)

38

LUPA: Late Upper Paleolithic specimens from North Africa LUPAE: North-East Esna, Jebel Sahaba (4, 10, 15, 16, 17, 19, 20, 21, 22, 23, 25, 26, 28, 31, 33, 38, 39, 42, 45, 102, and 106); Ohalo H2; Wadi Kubbaniya; Wadi Mataha F-81 LUPAW: North-West Afalou (1–3, 5, 7, 9, 10–15, 17, 18, 20, 22–25, 27–34, 36–38, 40, 42–44, 46–48) and Taforalt (I-a, VIII-fa; IX; X-CA; XI-C1; XI-C2; XII-C1; XII-C4; XIV; XV-C2; XV-C4; XV-C5; XVII-C2; XVII-C3; XX-C1; XXV-C1; XXV-C3; XXVII-C2; I-b; V; VIII; VIII-C; XIII; XVI-C1; XVI-C2; XVI-C3; XVII-C1; XIX-C1; XX-C2; XXIV-C1; XXIV-C2; XXV-2; XXV-C3b; XXV-C4; XXVII-C1)

97

NEAND: Classical Neandertal specimens from Eurasia Europe Arcy-sur-Cure 9; Cova Negra; Feldhofer 1; Gibraltar 1; Guattari 1; La Chapelle-aux-Saints 1; La Ferrassie 1; La Quina 5; Le Moustier 1; Regourdou 1; Saccopastore 1; Sˇala 1; Salzgitter-Lebenstedt 1; Spy (I and II). Southwest Asia Amud 1; Kebara 2; Shanidar (1, 2, 4, and 5); and Tabun (1 and 2)

23

TABLE 3. List of the archaic and morphometric features displayed by the Nazlet Khater 2, Oase, and Hofmeyr fossils

Archaic features associated to a powerful masticatory system Cranial vault thickness (Lieberman, 1996; Balzeau, 2005) Developed maxillar tuberosities (Enlow, 1990; Varrela, 1992) Strong phenozygy (ibidem) Large facial height (ibidem) Large facial width (ibidem) Postglenoid tubercle height (Elyaqtine, 1995) Relatively anteriorly positioned zygomatic bones w/ anterior zygomatic root mesial of the M1s (on NK2 and Oase 2) or above M1 (Maureille, 1994) Broad ramus, absolutely and relative to mandibular length (Bastir et al., 2004) Large teeth/Molar megadontia Unusual molar size progression: M1 \ M2 \ M3 (Very) complex enamel arrangement of the M3s Archaic metrical features, independent? Flat frontal arc (particularly compared to the parietal arc) Frontal obliquity Parietal arc shorter than frontal arc Occipital arc longer than parietal arc Archaic morphological features, independent? Low position of the maximum cranial breadth Triangular shape of temporal squama (form 1 after Elyaqtine, 1995) Linear parietal border of temporal squama Prolongation of supra-mastoid crests onto the parietal (Elyaqtine, 1995) Anterior bridge on digastric groove Medial position of styloid process to the digastric groove and stylo-mastoid foramen Relatively large juxtamastoid eminence Supraorbital relief continuous Prominent glabella (grade IN after Lahr, 1996) Broad frontal process of the maxilla Geniogloss fossa and transverse tori on posterior face of mandibular symphysis Individual particularities Weak chin (mentum osseum rank after Dobson and Trinkaus, 2002) Mylohyoid bridging (bridge type) Planum triangulare Sutural ossicle at squamous suture, on parietal (flame shape) Neandertal feature? Mylohyoid bridging (‘‘Horizontal-oval’’ type)

NK 2

Oase 1

Oase 2

Hofmeyr

p p p p p (1) p (1) p

– – – – – – –

a a p a a a p

a – p p (1) p p p

p a a a

p p (1) p p

– p (1) p p

a p (1) a a

a p p p

– – – –

p (1) p a a

a a a –

p p p p p (rt) p (rt)

– – – – – –

a a (form2) p a a a

a p (?) p a – –

a – ‘‘a’’ (IN 2) a p

– – – – a

p a ‘‘a’’ (IN 2) p –

a p p (IN 4) p –

p (rank4) a p (lt) p (rt)

p (rank4) a a –

– – – p (lt)

– p (rt) p (rt) a

a

p (lt)

–

a (rt)

References that link the size of the masticatory system to the inventoried traits and those that refer to a grading scale are cited. p(1) indicates the presence of a strongly developed feature. rt, right; lt, left; p, present; a, absent.

American Journal of Physical Anthropology

LATE PLEISTOCENE HUMAN CRANIAL DIVERSITY (39%, n 5 28) in the African Epipaleolithic samples from Wadi Halfa and Jebel Sahaba (Crevecoeur, 2008). The squamous temporal of NK 2 exhibits a triangular outline (‘‘shape 1’’ of Elyaqtine, 1995), which may be considered as an archaic feature, as it is present in Asian archaic Homo (Weidenreich, 1936). It is also exhibited by Qafzeh 9 (Vandermeersch, 1981). This configuration is quite rare in recent human populations, except among the Inuit (Elyaqtine, 1995). HOF also possesses a straight parietal border, but its squama is very high and the junction between the sphenoid and parietal borders—now broken—had a rather peculiar divided apex (Grine et al., 2007). The petrous temporal of NK 2 exhibits two morphological features that are unusual among modern humans. The digastric groove is not symmetrical; on the right, it is closed anteriorly by a bony bridge joining the internal side of the mastoid process with the petrous. This configuration is shown by the Ngaloba cranium (Elyaqtine, 1995), and it is common in archaic Homo and Neandertals (Vallois, 1969; Elyaqtine, 1995). On the same side, NK 2 presents an unusual medial position of the styloid process in relation to the axis defined by the digastric groove and the stylomastoid foramen. According to Elyaqtine (1995), this configuration is extremely rare among extant humans (\2%; n 5 140) and Upper Paleolithic specimens, but it is not uncommon in earlier Homo fossils (e.g., Sale´, Omo 2, and Skhul V) and among Neandertals. The juxtamastoid eminence of OAS 2 is well developed, but the mastoid process projects further inferiorly. Various degrees of development of the juxtamastoid eminence have been observed among archaic Homo and later specimens, but in no instance it has been observed to project beyond the level of the mastoid process, as is the case among Neandertals (Elyaqtine, 1995). HOF presents a continuous supraorbital torus. This is an exceedingly rare morphology among living humans (Lahr, 1996), but is exhibited by the Skhul and Jebel Irhoud specimens (Vandermeersch, 1981; Hublin, 1993). Although the Upper Paleolithic Mladecˇ 5 cranium has been said to possess a continuous supraorbital torus (Frayer et al., 2006), our observations of the specimen (FEG) are in agreement with those of Smith (1984), who noted the presence of a supraorbital sulcus separating a prominent medial supraorbital swelling from a thick lateral superciliary arch. As such, the robust brow exhibited by Mladecˇ 5 is not a true torus, as defined by Smith and Ranyard (1980). With reference to the mandible, only NK 2 and OAS 1 preserve the symphysis. In section, the two show different morphologies. OAS 1 has no torus, whereas NK 2 possesses pronounced inferior and superior transverse tori that are separated by a deep glenioglossal fossa (Crevecoeur and Trinkaus, 2004). This configuration has been described for Asian archaic Homo (Weidenreich, 1936) and Neandertals (Ali, 2005), and it is also exhibited by Skhul V and Qafzeh 9 (Vandermeersch, 1981). It is present in about 10% of recent humans (Ali, 2005), but absent from the Late Upper Paleolithic sample from North Africa (LUPA; n 5 75). Trinkaus et al. (2003) reported the presence of the ‘‘horizontal-oval’’ type of mandibular foramen (Kallay, 1970; Smith, 1978) on the left side of OAS 1, although it is absent from the opposite side. It is also absent from the NK 2 and HOF mandibular rami. The incidence of the ‘‘horizontal-oval’’ foramen in recent human populations is very low, at about 5% (Yamano and Yamaguchi, 1976), whereas a much higher frequency, approaching 50%, has

351

been observed for Neandertals (Jidoi et al., 2000). An incidence of 11.8% has been reported for a sample of Upper Paleolithic Europeans (Soficaru et al., 2006), and we observed a somewhat higher frequency (18.5%) in the Iberomaurusian sample (n 5 27) from Taforalt.

Univariate and bivariate analyses of morphometric variation In the dimensions of the neurocranium and face, each of the three fossils exhibits different characteristics with respect to the comparative samples (Table 4). They lie variously outside the ranges of variation of these groups for different variables, which underscores their distinctive and particular morphologies. We focus here on several of these features. Size is not the only factor that accounts for the position of NK 2, HOF, and OAS in comparison to the other Late Pleistocene samples. The transversal craniofacial index (ICT) value for NK2, which reflects an extremely broad face in relation to the neurocranium (see Fig. 3), falls beyond all of the Pleistocene sample ranges. At the same time, the index values of OAS 2 and HOF fall within the ranges of variation for all of the Pleistocene samples. With regard to the metrical features that describe the sagittal curvature of the frontal, OAS 2 and HOF show opposite configurations. A flat frontal arc, particularly in comparison to the parietal curvature, characterizes OAS 2 (Rougier et al., 2007). Its sagittal frontal index (ICF) value is beyond the ranges of the Early and Later Upper Paleolithic (EUP and LUPA) samples, whereas the sagittal parietal index (ICP) value for HOF falls outside the ranges of these two samples (see Fig. 4). Figure 4 also illustrates the flat frontals and parietals of Neandertals in comparison to the individuals comprising the European Upper Paleolithic (EUP) sample. With regard to the bregmatic angle of Schwalbe, which portrays the angle formed from bregma to glabella and inion (see Fig. 5), Neandertals are seen to be quite distinct, with obliquely oriented frontals in comparison to the more vertical frontals in the other samples. The value for OAS 2 falls within the lower part of the EUP range of variation, and NK 2 has an even more acute bregmatic angle. In the proportions of the frontal, parietal, and occipital arcs, NK 2 has an unusual disposition among recent humans; its frontal is longer than the parietal, which is, in turn, shorter than the occipital (Crevecoeur, 2008). HOF shares with NK 2 the greater length of the frontal than the parietal, a configuration that is quite common, with between 42.9 and 63.6% of individuals comprising the comparative samples displaying it (Table 5). On the other hand, the relative lengths of the occipital and parietal seen in NK 2 are very frequent among Neandertals, but present in only about 15% of the individuals comprising the MPHS and EUP samples, and even rarer among LUPA crania (Table 5). Finally, the configuration exhibited by NK 2, in which frontal [ occipital [ parietal, is seen with less frequency in the EUP and LUPA samples. It is exhibited by Skhul IX, and is a common feature among archaic Homo crania (Hublin, 1991). As such, it might be regarded as an archaic trait. The NK 2 and OAS 1 mandibles have remarkably broad rami (see Fig. 6), a feature that Bastir et al. (2004) have argued may be related to more than just the strength of the masticatory apparatus. In relation to American Journal of Physical Anthropology


187.0 136.0 95.0 122.0 113.3 130.1 115.8 117.8 116.0 105.0 54.0 148.0 72.2 43.7 36.1 27.2 56.8 100.5 51.0 89.2 90.7 108.8

NK 2

194.0 138.0 97.5 110.9 117.2 130.5 134.5 124.0 120.7 119.5 56.1 132.4 69.0 46.4 31.5 25.5 47.8 95.0 46.2 92.5 88.8 95.9

OAS 1–2

40.0 86.2 94.4 93.9

138.0 77.0 41.0 31.0 31.0 51.0

112.0 118.0

194.0 147.0 99.5 117.0 118.2 130.0 125.0

HOF

12 13 12 10 8 10 13 7 12 14 5 8 8 7 7 8 8 3 3 10 13 7

n

MPHS

182.5 140.0 96.0 112.0 112.0 118.0 120.0 120.0 106.0 96.0 54.3 134.0 69.0 41.8 29.4 27.0 46.0 87.0 35.9 85.7 89.0 83.2

min 219.5 161.0 117.0 131.0 124.1 142.0 145.0 129.0 124.3 129.0 66.0 160.0 79.0 48.0 41.0 33.0 56.0 103.0 41.7 93.6 96.9 108.1

max – \ \ – – – \ \ – – \ – – – – – [ – [ – – [

NK 2 – \ – \ – – – – – – – \ – – – \ – – [ – \ –

OAS 1–2

– – – –

– – \ – – –

– –

– – – – – – –

HOF 32 36 31 32 26 33 34 26 34 33 13 17 23 22 26 27 23 11 11 32 33 17

n

EUP

178.0 130.0 92.0 113.0 105.7 121.0 117.0 110.0 103.0 107.0 54.0 126.0 59.1 38.0 26.0 22.0 44.1 80.0 34.2 81.0 86.4 93.1

min 211.0 166.5 111.1 138.5 132.0 148.0 156.5 134.0 132.0 143.1 67.5 156.0 78.0 48.3 36.5 30.0 59.0 100.0 42.6 90.3 95.9 103.3

max – – – – – – \ – – \ – – – – – – – [ [ – – [

NK 2 – – – \ – – – – – – – – – – – – – – [ [ – –

OAS 1–2

– – – –

– – – – [ –

– –

– – – – – – –

HOF 83 83 80 71 74 78 80 69 45 49 32 64 67 71 70 63 63 50 51 45 49 62

n

LUPA

173.0 126.0 82.0 101.1 98.0 110.0 111.7 102.8 98.0 106.0 51.0 117.0 57.0 37.0 27.0 22.0 44.0 67.5 29.6 82.6 86.4 84.8

min 206.5 159.0 114.0 135.0 129.0 147.0 153.0 140.0 123.0 138.0 67.0 152.0 74.0 46.0 36.0 31.5 63.5 96.0 46.5 92.0 94.9 108.6

max – – – – – – – – – \ – – – – [ – – [ [ – – [

NK 2 – – – – – – – – – – – – – [ – – – – – [ – –

OAS 1–2

– – – –

– [ – – – –

– –

– – – – – – –

HOF 12 13 13 14 11 13 12 8 13 13 12 9 8 8 9 9 8 9 9 13 12 7

n

181.0 138.5 101.1 114.0 102.2 110.0 105.0 110.0 102.8 103.2 44.0 134.0 80.4 45.0 36.1 30.2 57.0 85.0 37.2 86.3 90.6 89.9

min

max 215.0 160.0 119.0 128.0 121.0 135.0 131.0 133.0 120.0 118.8 53.0 160.0 94.0 49.1 39.0 38.5 68.5 112.0 45.5 95.5 107.1 99.1

NEAND

– \ \ – – – – – – – [ – \ \ – \ \ – [ – – [

NK 2

– \ \ \ – – [ – [ [ [ \ \ – \ \ \ – [ – \ –

OAS 1–2

– \ – –

– \ \ \ – \

– –

– – \ – – – –

HOF

a

Arrows indicate a value of NK 2, OAS 1 and 2, or HOF that falls out of the comparative ranges (inferior ‘‘\’’, superior ‘‘[’’). Abbreviations following Howells, 1973 (GOL, maximum cranial length; XCB, maximum cranial breadth; XFB, maximum frontal breadth; FRC, frontal sagittal chord; PAC, parietal sagittal chord; ZYB, zygomatic breadth; NPH, upper facial height; OBH, orbital height; NLB, nasal breadth; NLH, nasal height). b Abbreviations referring to Martin’s measurements [BFT 5 M9, least frontal breadth; ABH 5 M20, auriculo-bregmatic height; FAR 5 M26, frontal sagittal arc; PAR 5 M27, parietal sagittal arc; OAR 5 M28, occipital sagittal arc; SWA 5 M32(2), bregmatic angle of Schwalbe; MEB 5 M51, orbital breadth; LCM 5 M68, projective length of the corpus mandibulae; RMB 5 M71a, minimum anteroposterior width of the ramus; ICF 5 I.22, sagittal frontal index (FRC/FAR); ICP 5 I.24, sagittal parietal index (PAC/PAR); ICT 5 I.71, transversal cranio-facial index (ZYB/XCB)].

GOL XCBa BFTb XFBa ABHb FARb PARb OARb FRCa PACa SWAb ZYBa NPHa MEBb OBHa NLBa NLHa LCMb RMBb ICFb ICPb ICTb

a

Code

TABLE 4. Cranial and mandibular dimensions of Nazlet Khater 2, Oase 1 and 2, and Hofmeyr compared to the range of variation of the comparative samples

352 I. CREVECOEUR ET AL.

353

LATE PLEISTOCENE HUMAN CRANIAL DIVERSITY

Fig. 3. Box and whisker plots of the transversal craniofacial index (ICT) in the NK 2, Oase 2, and Hofmeyr crania and the comparative samples. Boxes display the median, 25th–75th and 5th–95th percentiles. NEAND, Neandertal (n 5 7); MPHS, Middle Pleistocene Homo sapiens (n 5 7); EUP, European Upper Paleolithic modern humans (n 5 17); LUPAW, North-West African Late Upper Paleolithic (n 5 44); LUPAE, North-East African Late Upper Paleolithic (n 5 19).

Fig. 5. Box and whisker plots of the Bregmatic angle of Schwalbe (SWA) in NK 2, Oase 2, and the comparative samples. Box plots display the median, 25th–75th and 5th–95th percentiles. Comparative sample abbreviations as in Figure 3. NEAND (n 5 12), MPHS (n 5 5), EUP (n 5 13), and LUPA, North African Late Upper Paleolithic (n 5 32). TABLE 5. Percentage of the individuals for each comparative group (sample abbreviations as in Figs. 3 and 5) with a frontal arc longer than the parietal arc (Fr > Pa), an occipital arc longer than the parietal arc (Oc > Pa), and the combination Fr > Oc > Pa % Fr[Pa NEAND MPHS EUP LUPA

% Oc[Pa

% Fr[Oc[Pa

NK2, HOF

N

NK2

N

NK2

N

63.6 42.9 54.5 43.4

11 7 33 76

85.7 16.7 15.4 10.3

7 6 26 68

42.9 25.0 11.5 1.5

7 4 26 68

The disposition of NK 2 and Hofmeyr (HOF) is indicated.

Multivariate analyses of variation

Fig. 4. Bivariate plot of sagittal parietal index (ICP) versus sagittal frontal index (ICF). Comparative sample abbreviations as in Figure 3.

mandibular corpus length, OAS 2 occupies a marginal position in comparison to the samples employed here, and NK 2 is even more distinctive in this regard.

The dimensions of the NK 2, OAS 2, and HOF neurocrania were compared to the Late Pleistocene fossil sample by PCAs on raw and size-adjusted measurements. Both yielded consistent results, signifying that dispersion of the specimens by principal components is independent of size. For this reason, only the PCAs on sizeadjusted neurocranial variables are illustrated (see Fig. 7). The dispersion according to the first two axes clearly distinguishes Neandertals from Middle to Late Upper Paleolithic humans. The majority of MPHS crania show an intermediate disposition between Neandertals and the later modern human groups. This is also the case of the EUP calotte of Mladecˇ 5. The neurocrania of NK 2, OAS 2, and HOF differ from one another, but all American Journal of Physical Anthropology

354


Fig. 6. Bivariate plot of minimum rameal width (RMB) against the projective length of the mandibular corpus (LCM). Comparative sample abbreviations as in Figure 3.

Fig. 8. Scatter plot of the first two principal components of the PCA computed on raw facial variables. Comparative sample abbreviations as in Figure 3.

Fig. 7. Scatter plot of the first two principal components of the PCA computed on size-adjusted neurocranial variables. Comparative sample abbreviations as in Figure 3.

Fig. 9. Scatter plot of the first two principal components of the PCA computed on size-adjusted facial variables. Comparative sample abbreviations as in Figure 3.

lie within the European and North African Upper Paleolithic ranges of diversity. With regard to variables of the facial skeleton, the raw and size-adjusted dimensions result in different specimen scatters. The dispersion of crania by raw measurements along the first axis is influenced mainly by size (see Fig. 8). All six variables are positively correlated with the first PC, and group dispersion follows a general trend of reduction of facial dimensions with time. In this regard, NK 2 and HOF possess high values, comparable to those of the chronologically earlier MPHS sample, and this speaks to their large size (Lieberman, 1996; Friess, 1999). OAS 2 lies within the range of Upper Paleolithic variation and occupies a position near Mladecˇ 1. In the size-adjusted measurements, NK 2 and HOF fall within

the ranges of Upper Paleolithic variation, whereas OAS 2 stands apart from the others because its orbits are wide in comparison to its nasal aperture (see Fig. 9). HOF, NK 2, and OAS 2 show considerable divergence with regard to the size and shape of the facial skeleton. To address the probability of encountering this level of variation between three individuals within the comparative samples, we computed the squared Mahalanobis distances of each individual (OAS 2, HOF, and NK 2) from the recent human centroid based on eight craniofacial dimensions. We then sampled three individuals using 10,000 resamplings and computed the sum of their distances from the living population sample. The histograms of the dispersions for the recent samples and for a sample of Late Pleistocene European and African speci-


355

LATE PLEISTOCENE HUMAN CRANIAL DIVERSITY

Fig. 10. Histogram of the frequency of the sum of squared Mahalanobis distances drawn during a random resampling (10,000 iterations with replacement) of three individuals among the recent human populations (Holocene sample) and a Late Pleistocene sample of African and European specimens (EUP and LUPA; n 5 62). The black line illustrates the sum of distances for NK 2, Oase 2, and Hofmeyr with the P-value related to the probability to draw it from the recent human sample dispersion.

TABLE 6. Univariate statistics of the two resampling dispersions obtained for recent (R) and Late Pleistocene populations (EUP and LUPA)

Mean Minimum Maximum Standard deviation Number Skewness Kurtosis Shapiro-Wilk F-Snedecor

Recent populations (R)

Late Pleistocene (LP; EUP and LUPA)

17.6745 2.9654 55.6229 6.5979 10000 0.8879 1.2224 W 5 0.9584

31.6983 5.9721 88.2160 11.4537 10000 0.9011 1.2478 W 5 0.9577

Test t (Welch) P-value (NK-O-H)

Normality hypothesis cannot be excluded F 5 3.0132 (P 5 0.00) Variances are different : LP [ R t 5 2105.966 (P 5 0.00) Means are different : LP [ R

0.0952

0.3567

The results of the Shapiro-Wilks Normality test, of the equivalence of variance (F-Snedecor) and mean tests (Welch’s t-test) as well as the probability (P-value) to sample the sum of squared Mahalanobis distances shown by NK 2, Oase 2, and Hofmeyr (NK-O-H) from each group are included.

mens (EUP and LUPA) are compared in Figure 10. The probability of randomly sampling the degree of variation expressed among NK 2, OAS 2, and HOF among recent populations is small (P 5 0.0952), whereas it is close to the average diversity observed within the combined Upper Paleolithic sample. Statistical comparison of the Holocene and Late Pleistocene dispersions is provided in Table 6. Although both histograms are normally distributed, the means and variances of the two resampling groups differ significantly. The results of the Welch’s ttest and the F-Snedecor’s test show that the mean and variance of the Late Pleistocene distribution are significantly greater than those of the Holocene sample (Table 6). This is also true when the EUP and the LUPA samples are individualized, and random resampling is performed separately, although the EUP sample shows a wider variation range than the LUPA sample. When applied to extant human populations, only the Khoe-San sample exhibits a greater range of variation than the other recent groups, but it is lower than the Pleistocene sample ranges.

DISCUSSION AND CONCLUSIONS The specimens from NK 2, OAS, and HOF provide a glimpse of Late Pleistocene human phenotypic diversity. These penecontemporaneous but geographically disparate individuals derive from a period (MIS 3) that witnessed modern human expansion into Eurasia and back into northern Africa from eastern Africa (Olivieri et al., 2006). Morphometric analyses suggest considerable diversity among these and other Late Pleistocene human crania. NK 2, OAS, and HOF exhibit individual characteristics by which they fall beyond the ranges of variation of other Pleistocene samples, and the multivariate analyses reveal that although their neurocrania exhibit an overall modern configuration, the facial dimensions of NK 2 and HOF suggest a more archaic disposition. Comparison of the variation among these three specimens with that exhibited among other Pleistocene and recent human samples highlights the greater phenotypic diversity in the Late Pleistocene. This suggests that the phe-


356


notypic diversity that characterized humans in the Late Pleistocene has been reduced in the Holocene. The results of the bootstrap analyses conducted in this study are compatible with the suggestion from genetic studies that living humans represent only a restricted part of past modern human variation (Underhill et al., 2000; Excoffier, 2002; Marth et al., 2003; Fagundes et al., 2007). Certainly the European and North African Upper Paleolithic samples appear to exhibit greater craniometric variability than recent human samples. Our results appear to accord with the conclusions reached by Manica et al. (2007), von Cramon-Taubadel and Lycett (2008), and Betti et al. (2009) regarding the proportional relationship between recent within-population craniometric diversity and geographic distance from eastern Africa. Despite a manifestly incomplete fossil record, the specimens that date from MIS 3 provide important information regarding the biological processes behind the emergence of modern humans. They provide a glimpse of the degree of morphological variability that appears to have characterized humanity in the Late Pleistocene.

ACKNOWLEDGMENTS The study of Nazlet Khater 2 has been made possible by the entrusting of this specimen for analysis to I.C. by P. Vermeersch, P. Van Peer, and B. Maureille. E. Trinkaus provided useful comments on this manuscript, and the authors thank P. Semal for assistance with the statistical analyses. We are grateful to the following curators and researchers who allow us to examine original fossils and collections in their care: H. de Lumley, D.L. Greene, D. Grimaud-Herve´, M. Judd, R. Kruszynski, N. Spencer, C. Stringer, M. Teschler-Nicola, D. Van Gerven. They also thank the anonymous referees for their comments, which substantially improved the manuscript.

LITERATURE CITED Ali R. 2005. La variabilite´ morphologique et me´trique de la symphyse et des structures mentonnie`res dans les populations actuelles et chez les hommes fossiles. Ph.D. thesis, Universite´ Bordeaux 1, France. Ambrose SH. 1998. Chronology of the Later Stone Age and food production in East Africa. J Archaeol Sci 25:377–392. Balzeau A. 2005. Spećificite´ des caracte`res morphologiques internes du squelette ce´phalique chez Homo erectus. Ph.D. thesis, Museúm National d’Histoire Naturelle, France. Barker G, Barton H, Bird M, Daly P, Datan I, Dykes A, Farr L, Gilbertson D, Harrisson B, Hunt C, Higham T, Kealhofer L, Krigbaum J, Lewis H, McLaren S, Paz V, Pike A, Piper P, Pyatt B, Rabett R, Reynolds T, Rose J, Rushworth G, Stephens M, Stringer C, Thompson J, Turney C. 2007. The ‘human revolution’ in lowland tropical Southeast Asia: the antiquity and behavior of anatomically modern humans at Niah Cave (Sarawak, Borneo). J Hum Evol 52:243–261. Bastir M, Rosas A, Kuroe K. 2004. Petrosal orientation and mandibular ramus breadth: evidence for an integrated petroso-mandibular developmental unit. Am J Phys Anthropol 123:340–350. Behar DM, Villems R, Soodyall H, Blue-Smith J, Pereira L, Metspalu E, Scozzari R, Makkan H, Tzur S, Comas D, Bertranpetit J, Quintana-Murci L, Tyler-Smith C, Wells RS, Rosset S; The Genographic Consortium. 2008. The dawn of human matrilineal diversity. Am J Hum Genet 82:1130– 1140. Betti L, Balloux F, Amos W, Hanihara T, Manica A. 2009. Dis-


tance from Africa, not climate, explains within-population phenotypic diversity in humans. Proc R Soc B 276:809–814. Braüer G. 1988. Osteometrie. In: Martin R, Knussmann R, editors. Handbuch der vergleichenden Biologie des Menschen (Band I, 1. Teil). Stuttgart: Gustav Fischer Verlag. p 160– 232. Braüer G, Singer R. 1996. The Klasies zygomatic bone: archaic or modern? J Hum Evol 30:161–165. Buyle-Bodin Y, Philippe M. 1982. L’anthropologie lyonnaise et la collection de craˆnes modernes rhoˆne-alpins du museé Guimet d’Histoire naturelle de Lyon: historique et geńe´ralite´s. Nouv Arch Mus Hist Natur Lyon 20:5–8. Clark JD, Beyene Y, Woldegabriel G, Hart WK, Renne PR, Gilbert H, Defleur A, Suwa G, Katoh S, Ludwig KR, Boisserie J-R, Asfaw B, White TD. 2003. Stratigraphic, chronological and behavioural contexts of Pleistocene Homo sapiens from Middle Awash, Ethiopia. Nature 423:747–752. Corruccini R. 1992. Metrical reconsideration of the Skhul IV and IX and Border Cave 1 crania in the context of modern human origins. Am J Phys Anthropol 87:433–445. ´ tude anthropologique du squelette du Crevecoeur I. 2008. E ´ gypte). Apport a` Paleólithique supe´rieur de Nazlet Khater 2 (E la compre´hension de la variabilite´ passeé des hommes modernes. Leuven: Egyptian Prehistory Monographs 8. Crevecoeur I, Trinkaus E. 2004. From the Nile to the Danube: a comparison of the Nazlet Khater 2 and Oase 1 early modern human mandibles. Anthropologie (Brno) 42:229–239. Crewdson-Benington R. 1911. Cranial type-contours. Biometrika 8:139–201. Darroch JN, Mosimann JE. 1985. Canonical and principal components of shape. Biometrika 72:241–252. Day MH, Leakey MD, Magori C. 1980. A new hominid fossil skull (L.H. 18) from the Ngaloba Beds, Laetoli, Northern Tanzania. Nature 284:55–56. Day MH, Stringer CB. 1982. A reconsideration of the Omo Kibish remains and the erectus-sapiens transition. In: de Lumley MA, editor. L’Homo erectus et la place de l’Homme de Tautavel parmi les hominide´s fossiles (Tome II). Paris: CNRS. p 814–846. Dean D, Hublin JJ, Holloway R, Ziegler R. 1998. On the phylogenetic position of the pre-Neandertal specimen from Reilingen, Germany. J Hum Evol 34:485–508. Demeter F, Manni F, Coppens Y. 2003. Late Upper Pleistocene human peopling of the Far East: multivariate and geographic patterns of variation. C R Palevol 2:625–638. Demoulin F. 1972. Le craˆne des Alge´riens. Ph.D. thesis, Universite´ de Paris VII, France. Dobson S, Trinkaus E. 2002. Cross-sectional geometry and morphology of the mandibular symphysis in Middle and Late Pleistocene Homo. J Hum Evol 43:67–87. Elyaqtine M. 1995. Variabilite´ et e´volution de l’os temporal chez Homo sapiens. Comparaison avec Homo erectus. Ph.D. thesis, Universite´ Bordeaux 1, France. Enlow DH. 1990. Facial growth, 3rd ed. Philadelphia: W. B. Saunders. Excoffier L. 2002. Human demographic history: refining the recent African origin model. Curr Opin Genet Dev 12:675–682. Fagundes NJR, Ray N, Beaumont M, Neuenschwander S, Salzano FM, Bonatto SL, Excoffier L. 2007. Statistical evaluation of alternative models of human evolution. Proc Natl Acad Sci USA 104:17614–17619. Field JS, Lahr MM. 2005. Assessment of the southern dispersal: GIS-based analyses of potential routes at Oxygen Isotopic Stage 4. J World Prehist 19:1–45. Field JS, Petraglia MD, Lahr MM. 2007. The southern dispersal hypothesis and the South Asian archaeological record: examination of dispersal routes through GIS analysis. J Anthropol Archaeol 26:88–108. Frayer DW, Jelıńek J, Oliva M, Wolpoff MH. 2006. Aurignacian male crania, jaws and teeth from Mladecˇ caves, Moravia, Czech Republic. In: Teschler-Nicola M, editor. Early modern humans at the Moravian Gate. The Mladecˇ Caves and their remains. Wien: Springer-Verlag. p 185–272. Friess M. 1999. Some aspects of the cranial size and shape, and

LATE PLEISTOCENE HUMAN CRANIAL DIVERSITY their variation among later Pleistocene hominids. Anthropologie 37:239–246. Garrigan D, Hammer MF. 2006. Reconstructing human origins in the genomic era. Nature Rev Genet 7:669–680. Gonder MK, Mortensen HM, Reed FA, de Sousa A, Tishkoff SA. 2007. Whole-mtDNA genome sequence analysis of ancient African lineages. Mol Biol Evol 24:757–768. Grimaud D. 1982. Evolution du parie´tal de l’Homme fossile, position de l’Homme de Tautavel parmi les hominide´s. Ph.D. thesis, Museúm National d’Histoire naturelle, France. Grine FE, Bailey RM, Harvati K, Nathan RP, Morris AG, Henderson GM, Ribot I, Pike AWG. 2007. Late Pleistocene human skull from Hofmeyr, South Africa, and modern human origins. Science 315:226–229. Haile-Selassie Y, Asfaw B, White TW. 2004. Hominid cranial remains from Upper Pleistocene deposits at Aduma, Middle Awash, Ethiopia. Am J Phys Anthropol 123:1–10. Handley LJL, Manica A, Goudet J, Balloux F. 2007. Going the distance: human population genetics in a clinal world. Trends Genet 23:432–439. Howells WW. 1989. Skull shapes and the map: craniometric analysis in the dispersion of modern Homo. Papers of the Peabody Museum. Cambridge: Harvard University Press. Hublin J-J. 1991. L’e´mergence des Homo sapiens archaı¨ques: Afrique du nord-ouest et Europe occidentale. The`se d’Etat, Universite´ Bordeaux 1, France. Hublin J-J. 1993. Recent human evolution in northwestern Africa. In: Aitken MJ, Stringer CB, Mellars PA, editors. The origin of modern humans and the impact of chronometric dating. New Jersey: Princeton University Press. p 118–131. Ingman M, Kaessmann H, Paä¨bo S, Gyllensten U. 2000. Mitochondrial genome variation and the origin of modern humans. Nature 408:708–713. Jidoi F, Nara T, Dodo Y. 2000. Bony bridging of the mylohyoid groove of the human mandible. Anthropol Sci 108:345– 370. Jungers WL, Falsetti AB, Wall CE. 1995. Shape, relative size, and size-adjustments in morphometrics. Yearbk Phys Anthropol 38:137–161. Kallay J. 1970. Komparativne napomene o cˇeljustima Krapinskih praljudi obzirom na polozˇaj med-u Hominidima. In: Malez M, editor. Krapina 1899–1969. Zagreb: Jugoslavenske Akademije Znanosti I Umjetmosti. p 153–164. Kidder JH, Jantz RL, Smith FH. 1992. Defining modern humans: a multivariate approach. In: Braüer G, Smith FH, editors. Continuity or replacement? Controversies in Homo sapiens evolution. Rotterdam: AA Balkema. p 157–177. Krogman W, Schmidt E. 1933. The Alishar Huÿu¨k Seasons of 1928 and 1929. Chicago: The University of Chicago Press. Lahr MM. 1996. The evolution of modern human diversity: a study of cranial variation. Cambridge: Cambridge University Press. Li JZ, Absher DM, Tang H, Southwick AM, Casto AM, Ramachandran S, Cann HM, Barsh GS, Feldman M, Cavalli-Sforza LL, Myers RM. 2008. Worldwide human relationships inferred from genome-wide patterns of variation. Science 319:1100– 1104. Lieberman DE. 1996. How and why humans grow thin skulls: experimental evidence for systemic cortical robusticity. Am J Phys Anthropol 101:217–236. Lieberman DE, McBratney BM, Krovitz G. 2002. The evolution and development of cranial form in Homo sapiens. Proc Natl Acad Sci USA 99:1134–1139. Liu H, Prugnolle F, Manica A, Balloux F. 2006. A geographically explicit genetic model of worldwide human-settlement history. Am J Hum Genet 79:230–237. Lohmueller KE, Indap AR, Schmidt S, Boyko AR, Hernandez RD, Hubisz MJ, Sninsky JJ, White TJ, Sunyaev SR, Nielsen R, Clark AG, Bustamante CD. 2008. Proportionally more deleterious genetic variation in European than in African populations. Nature 451:994–998. Macaulay V, Hill C, Achilli A, Rengo C, Clarke D, Meehan W, Blackburn J, Semino O, Scozzari R, Cruciani F, Taha A, Shaari NK, Raja JM, Ismail P, Zainuddin Z, Goodwin W,

357

Bulbeck D, Bandelt H-J, Oppenheimer S, Torroni A, Richards M. 2005. Single, rapid coastal settlement of Asia revealed by analysis of complete mitochondrial genomes. Science 308:1034–1037. Manica A, Amos W, Balloux F, Hanihara T. 2007. The effect of ancient population bottlenecks on human phenotypic variation. Nature 448:346–348. Marquer P. 1972. Nouvelle contribution a` l’e´tude du squelette des Pygmeés occidentaux du Centre africain compare´ a` celui ´ ditions du Museúm. des Pygmeés orientaux. Paris: E Marth G, Schuler G, Yeh R, Davenport R, Agarwala R, Church D, Wheelan S, Baker J, Ward M, Kholodov M, Phan L, Czabarka E, Murvai J, Cutler D, Wooding S, Rogers A, Chakravarti A, Harpending HC, Kwok P-Y, Sherry ST. 2003. Sequence variations in the public human genome data reflect a bottlenecked population history. Proc Natl Acad Sci USA 100:376–381. ´ tude de quatre squelettes de PygMatiegka J, Maly J. 1938. E meés centre-africains du bassin de l’Ituri. Anthropologie 48:521–538. Maureille B. 1994. La face chez Homo erectus et Homo sapiens: recherche sur la variabilite´ morphologique et me´trique. Ph.D. thesis, Universite´ Bordeaux 1, France. McDermott F, Gru¨n R, Stringer C, Hawkesworth CJ. 1993. Mass-spectrometric U-series dates for Israeli Neanderthal/ early modern hominid sites. Nature 363:252–255. McDougall I, Brown FH, Fleagle JG. 2005. Stratigraphic placement and age of modern humans from Kibish, Ethiopia. Nature 433:733–736. Mellars P. 2006a. Why did modern human populations disperse from Africa ca. 60,000 years ago? A new model. Proc Natl Acad Sci USA 103:9381–9386. Mellars P. 2006b. A new radiocarbon revolution and the dispersal of modern humans in Eurasia. Nature 439:931–935. Middleton GV. 2000. Data analysis in the earth sciences using Matlab. New Jersey: Prentice-Hall. Milicer-Gruzewska H. 1955. Crania Australica. Wroclaw: Panstowowe Wydawnictwo Naukowe. Olivieri A, Achilli A, Pala M, Battaglia V, Fornarino S, AlZahery N, Scozzari R, Cruciani F, Behar DM, Dugoujon JM, Coudray C, Santachiara-Benerecetti AS, Semino O, Bandelt HJ, Torroni A. 2006. The mtDNA legacy of the Levantine early Upper Palaeolithic in Africa. Science 314: 1767–1770. Quintana-Murci L, Semino O, Bandelt HJ, Passarino G, McElreavey K, Santachiara-Benerecetti AS. 1999. Genetic evidence of an early exit of Homo sapiens sapiens from Africa through eastern Africa. Nat Genet 23:437–441. Ribot I. 1998. Cranial variation in Equatorial Africa. M.Phil. dissertation, University of Cambridge, United Kingdom. Riquet R. 1953. La population des grottes de Baye. Bulletins et Me´moires de la Socie´te´ d’Anthropologie de Paris 4:45–67. Rougier H, Milota S , Rodrigo R, Gherase M, Sarcina L, Moldovan O, Zilhaõ J, Constantin S, Franciscus RG, Zollikofer CPE, Ponce-de-Leoń M, Trinkaus E. 2007. Pes tera cu Oase 2 and the cranial morphology of early modern Europeans. Proc Natl Acad Sci USA 104:1165–1170. Shang H, Tong H, Zhang S, Chen F, Trinkaus E. 2007. An early modern human from Tianyuan Cave, Zhoukoudian, China. Proc Natl Acad Sci USA 104:6573–6578. Shrubsall F. 1898. Crania of African Bush races. J R Anthropol Inst Great Britain Ireland 27:263–292. Smith F. 1984. Fossil hominids from the Upper Pleistocene of central Europe and the origin of modern Europeans. In: Smith F, Spencer F, editors. The origins of modern humans. A World Survey of the fossil evidence. New York: Alan R. Liss. p 137–209. Smith F, Ranyard G. 1980. Evolution of the supraorbital region in Upper Pleistocene Fossil Hominids from South-Central Europe. Am J Phys Anthropol 53:589–610. Smith FH. 1978. Evolutionary significance of the mandibular foramen area in Neandertals. Am J Phys Anthropol 48:523–532. Soficaru A, Dobos A, Trinkaus E. 2006. Early modern humans from Pes tera Muierii, Baia de Fier, Romania. Proc Natl Acad Sci USA 103:17196–17201.


358


STATlab. 1991. CNET-FranceTelecom-SLP. Version 2.1. Takasaka T, Kitamura T, Sugimoto C, Guo J, Zheng H-Y, Yogo Y. 2006. Phylogenetic analysis of major African genotype (Af2) of JC virus: implications for origin and dispersals of modern Africans. Am J Phys Anthropol 129:465–472. Thoma A. 1984. Morphology and affinities of the Nazlet Khater Man. J Hum Evol 13:287–296. Trinkaus E, Moldovan O, Milota S , Bıˆlgar A, Sarcina L, Athreya S, Bailey SE, Rodrigo R, Gherase M, Higham T, Ramsey CB, van der Plicht J. 2003. An early modern human from Pes tera Oase, Romania. Proc Natl Acad Sci USA 100: 11231–11236. Underhill PA, Kivisild T. 2007. Use of Y chromosome and mitochondrial DNA population structure in tracing human migrations. Ann Rev Genet 41:539–564. Underhill PA, Shen PD, Lin AA, Jin L, Passarino G, Yang W, Kauffman E, Bonne-Tamir B, Bertanpetit J, Francalacci P, Ibrahim M, Jenkins T, Kidd JR, Mehdi SQ, Seielstad MT, Wells RS, Piazza A, Davis RW, Feldman MW, Cavalli-Sforza L, Oefner PJ. 2000. Y chromosome sequence variation and the history of human populations. Nat Genet 26:358–361.


Vallois HV. 1969. Le temporal neándertalien H27 de La Quina. Etude anthropologique. L’Anthropologie 73:365–400. Vandermeersch B. 1981. Les hommes fossiles de Qafzeh (Israe¨l). Paris: Editions du CNRS. Varrela J. 1992. Dimensional variation of craniofacial structures in relation to changing masticatory-functional demands. Eur J Orthod 14:31–36. Vermeersch PM. 2002. Paleolithic quarrying sites in Upper and Middle Egypt. Leuven: Egyptian Prehistory Monograph 4. Von Cramon-Taubadel N, Lycett SJ. 2008. Human cranial variation fits iterative founder effect model with African origin. Am J Phys Anthropol 136:108–113. Weidenreich F. 1936. The mandible of Sinanthropus pekinensis: a comparative study. Pekin: The Geological Survey of China. White TD, Asfaw B, DeGusta D, Gilbert H, Richards GD, Suwa G, Howell FC. 2003. Pleistocene Homo sapiens from Middle Awash, Ethiopia. Nature 423:742–747. Yamano S, Yamaguchi B. 1976. On the mylohoid canal in the human mandible. Bull Nat Sci Mus Ser D 2:37–44.