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Journal of Human Evolution 62 (2012) 395e411

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Journal of Human Evolution

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Variation in enamel thickness within the genus Homo

Tanya M. Smith a,b,*, Anthony J. Olejniczak b, John P. Zermeno a, Paul Tafforeau c, Matthew M. Skinner b,Almut Hoffmann d, Jakov Radov�ci�c e, Michel Toussaint f, Robert Kruszynski g, Colin Menter h,Jacopo Moggi-Cecchi i, Ulrich A. Glasmacher j, Ottmar Kullmer k, Friedemann Schrenk l, Chris Stringer g,Jean-Jacques Hublin b

aDepartment of Human Evolutionary Biology, 11 Divinity Avenue, Harvard University, Cambridge, MA 02138, USAbDepartment of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, D-04103 Leipzig, Germanyc European Synchrotron Radiation Facility, 6 Rue Jules Horowitz, BP 220, 38043 Grenoble Cedex, FrancedMuseum für Vor- und Frühgeschichte, Schloss Charlottenburg e Langhansbau, Spandauer Damm 22, D-14059 Berlin, GermanyeCroatian Natural History Museum, Demetrova 1, 10000 Zagreb, CroatiafDirection de l’Archéologie, Service Public de Wallonie, 5100 Namur, BelgiumgDepartment of Palaeontology, The Natural History Museum, London SW7 5BD, United KingdomhDepartment of Anthropology and Development Studies, University of Johannesburg, PO Box 524, Auckland Park 2006, South AfricaiDipartimento di Biologia Evoluzionistica ‘Leo Pardi,’ Università di Firenze, via del Proconsolo, 12, 50122 Firenze, Italyj Institute of Earth Sciences, Ruprecht Karl University Heidelberg, D-69120 Heidelberg, GermanykDepartment of Paleoanthropology and Messel Research, Senckenberg Research Institute, D-60325 Frankfurt, GermanylDepartment of Vertebrate Paleontology, Institute for Ecology, Evolution, and Diversity, Johann Wolfgang Goethe University, Frankfurt, Germany

a r t i c l e i n f o

Article history:Received 1 July 2011Accepted 13 December 2011Available online 22 February 2012

Keywords:Human evolutionHominin tooth structureDental morphologyEarly HomoArchaic HomoNeanderthal

* Corresponding author.E-mail address: tsmith@fas.harvard.edu (T.M. Smit

0047-2484/$ e see front matter � 2012 Elsevier Ltd.doi:10.1016/j.jhevol.2011.12.004

a b s t r a c t

Recent humans and their fossil relatives are classified as having thick molar enamel, one of very fewdental traits that distinguish hominins from living African apes. However, little is known about enamelthickness in the earliest members of the genus Homo, and recent studies of later Homo report consid-erable intra- and inter-specific variation. In order to assess taxonomic, geographic, and temporal trendsin enamel thickness, we applied micro-computed tomographic imaging to 150 fossil Homo teeth span-ning two million years. Early Homo postcanine teeth from Africa and Asia show highly variable averageand relative enamel thickness (AET and RET) values. Three molars from South Africa exceed Homo AETand RET ranges, resembling the hyper thick Paranthropus condition. Most later Homo groups (archaicEuropean and north African Homo, and fossil and recent Homo sapiens) possess absolutely and relativelythick enamel across the entire dentition. In contrast, Neanderthals show relatively thin enamel intheir incisors, canines, premolars, and molars, although incisor AET values are similar to H. sapiens.Comparisons of recent and fossil H. sapiens reveal that dental size reduction has led to a disproportionatedecrease in coronal dentine compared with enamel (although both are reduced), leading to relativelythicker enamel in recent humans. General characterizations of hominins as having ‘thick enamel’ thusoversimplify a surprisingly variable craniodental trait with limited taxonomic utility within a genus.Moreover, estimates of dental attrition rates employed in paleodemographic reconstruction may bebiased when this variation is not considered. Additional research is necessary to reconstruct hominindietary ecology since thick enamel is not a prerequisite for hard-object feeding, and it is present in mostlater Homo species despite advances in technology and food processing.

� 2012 Elsevier Ltd. All rights reserved.

Introduction

Enamel thickness has been of considerable interest for studies offossil ape and human taxonomy, phylogeny, and paleodiet over thepast century. Radiographic comparisons of molar enamel thickness

h).

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were first employed in 1918 to argue that the PiltdownMan did notdisplay diagnostic human-like characters, as its thick molar enamelwas apparent in both living humans and orangutans (Miller, 1918).Despite validation of this early work, the taxonomic status of thick-enameled ‘Ramapithecus’ was debated for decades before it wasaccepted as a fossil ape rather than a human ancestor (Simons andPilbeam, 1972; Greenfield, 1974; Gantt, 1977; Andrews, 1982; Kay,1982; Lipson and Pilbeam, 1982; Ward and Pilbeam, 1983).Following the conclusion of this debate, Martin (1983) advocated

T.M. Smith et al. / Journal of Human Evolution 62 (2012) 395e411396

for the use of a size-corrected relative enamel thickness index(described below), which supported the prevailing view of homi-noid phylogeny and distinguished three recent groups: those withthin enamel (Pan, Gorilla), those with intermediate-thick enamel(Pongo), and those with thick enamel (Homo sapiens). Given thesedifferences, molar enamel thickness is among a small numberof features almost invariably reported in recent descriptions ofnew hominin fossils (reviewed in Olejniczak and Grine, 2006;Olejniczak et al., 2008d; Smith et al., 2008). Although enamelthickness is no longer regarded as a reliable phylogenetic characterdue to considerable homoplasy (Dumont, 1995; Begun and Kordos,1997; Schwartz, 2000; Smith et al., 2003; Olejniczak, 2006), taxo-nomic assessments of hominin enamel thickness continue to berelevant (e.g., Kono and Suwa, 2008; Smith et al., 2008; Olejniczaket al., 2008a, b, d; Suwa et al., 2009; Bayle et al., 2010; Benazzi et al.,2011a, b), as are studies of the relationship between primateenamel thickness and dietary ecology (e.g., Kono and Suwa, 2008;Vogel et al., 2008; Lucas et al., 2008a, b; Constantino et al., 2009).

Knowledge of hominin enamel thickness has been compli-cated by the limited fossil record and lack of accurate non-

Table 1Characterizations of enamel thickness reported for fossil hominin perman

Taxon Description

Sahelanthropus tchadensis IntermediateOrrorin tugenensis ThickArdipithecus kadabbaa IntermediateArdipithecus ramidus Thin & Intermediate

IntermediateAustralopithecus anamensisb Thick

ThickAustralopithecus afarensisb Thick

ThickAustralopithecus africanusb,c Thick

IntermediateParanthropus boiseid Thick & Hyper thick

Thick-Hyper thickParanthropus robustusb,c,e Thick-Hyper thick

ThickSouth African Homo sp. Thick & Very thickHomo erectus ThickHomo erectus/Homo habilisd Intermediate/ThickHomo neanderthalensis Thin

ThinThickIntermediateLarge

MSA Homo sapiens ThickThick

Early/UP Homo sapiensf Thick

Description: reported enamel thickness state. Note that intermediate molarthe thin end of the range) and humans or Australopithecus at the thick end (1aemicro-CT (voxel sizes< 50microns); 1bemedical grade CT (typical voflat-plane radiograph.

a Haile-Selassie (2001) reports as comparable to, or slightly greater thanb Suwa et al. (2009) give linear lateral enamel thickness values for Ar.

naturally-fractured teeth (and possibly some micro-CT scanned teeth) showdo not qualify enamel thickness in these taxa.

c Gantt (1986) includes measurements for naturally-fractured A. africanexceeds recent Homo. Sperber (1985, 1986) and Zilberman et al. (1990) givfrom flat-plane radiography, noting that the latter taxon is thicker, and that(1991) and Schwartz (1997) give linear and average enamel thickness meathe latter taxon is thicker, and that enamel thickness in both taxa exceeds rthat attempt to qualify enamel thickness from worn teeth.

d Beynon and Wood (1986) report that linear enamel thickness of natuguishes early Homo from P. boisei, but do not qualify thickness for either g(including KNM-ER 1802). Also, Ramirez Rozzi (1998) gives measuremenspecimens to taxa.

e Robinson (1956) gives linear thickness measurements for naturally-fracdoes not qualify thickness.

f Bayle et al. (2010) give 3D enamel thickness measurements for an Uppsimilarities to extant humans.

destructive methods of study. For example, the earliest-knownputative hominin genera, Sahelanthropus and Orrorin, are repre-sented by a small number of mostly worn and/or broken teeth(Senut et al., 2001; Brunet et al., 2002, 2005), prohibiting precisecharacterization of relative enamel thickness. Moreover, severaldisparate enamel thickness conditions have been reported forPliocene and early Pleistocene hominins, ranging from ‘thin’ to‘hyper-thick enamel’ (Table 1), although few studies employequivalent measurement criteria or qualitative distinctions.Studies of enamel thickness in the permanent dentition of fossilHomo species have been restricted to comparisons of Neanderthaland H. sapiens molars (e.g., Olejniczak et al., 2008a; Smith et al.,2009a; Bayle et al., 2010), with the exception of reports onnaturally-fractured east African early Homo postcanine teeth(Beynon and Wood, 1986; Ramirez Rozzi, 1998), two early Homomolars from South Africa (Schwartz, 1997), and four Asian Homoerectus molars (Smith et al., 2009b). While early Homo has beenreported to have thinner cuspal enamel than robust australopiths(Beynon and Wood, 1986, 1987; Ramirez Rozzi, 1998; but seeSchwartz, 1997; Tafforeau et al., 2011), studies of naturally-

ent molars.

Method References

1a, 1b Brunet et al., 2002, 20052 Senut et al., 20012 Haile-Selassie, 20012 White et al., 19941a Suwa et al., 20093 Ward et al., 20011a, 2 White et al., 20062 White et al., 19941a Macchiarelli et al., 20043 Grine and Martin, 19881a Olejniczak et al., 2008c2 Beynon and Wood, 19863 Grine and Martin, 19883 Grine and Martin, 19881a Olejniczak et al., 2008c1b Schwartz, 19971a Smith et al., 2009a2 Beynon and Wood, 19864 Zilberman and Smith, 19924 Molnar et al., 19931a Olejniczak and Grine, 20051a Olejniczak et al., 2008b1a Benazzi et al., 2011a, b1a Smith et al., 2006a1a Hublin et al., in press4 Zilberman and Smith, 1992

enamel thickness is often described as that between chimpanzees (ate.g., White et al., 1994; Brunet et al., 2002; Suwa et al., 2009). Method:xel sizes>200microns); 2e natural fracture; 3e physical section; 4e

Ar. ramidus.ramidus, A. anamensis, A. afarensis, A. africanus, and P. robustus froming an increase in absolute values from the first to the last taxon, but

us and P. robustus teeth, reporting that enamel thickness in both taxae linear thickness measurements for A. africanus and P. robustus teethenamel thickness in both taxa exceeds recent Homo. Similarly Conroysurements for A. africanus and P. robustus from medical CT, noting thatecent Homo. Also see Beynon andWood (1986) for a review of studies

rally-fractured east African Plio-Pleistocene teeth significantly distin-roup save for two exceptional early Homo specimens that are ‘thick’ts for naturally-fractured east African hominins but does not assign

tured P. robustus, noting that A. africanus does not differ markedly, but

er Paleolithic modern human permanent molar from micro-CT, noting

Table 2Hominin dental material included in this study.

Taxon I1 I2 C P3 P4 M1 M2 M3 Total

East African early Homoa e e 1 2 2 2 2 e 9South African early Homo e e e 1 e 2 1 e 4Asian Homo erectus e e e 2 2 2 1 3 10Archaic European Homo e e e e 1 1 1 2 5Archaic North African Homo e e e 2 1 e 1 1 5Homo neanderthalensis 8 8 6 5 6 22 12 11 78Fossil Homo sapiens 4 5 6 4 3 10 5 2 39Recent Homo sapiens 48 43 42 36 43 98 76 97 483

A complete list of fossil specimens is given in Appendix A.a B. Wood currently attributes these specimens to Homo habilis or Homo rudol-

fensis (pers. com.).

T.M. Smith et al. / Journal of Human Evolution 62 (2012) 395e411 397

fractured teeth are prone to error due to section plane obliquity(Martin, 1983).

Numerous studies have also suggested that enamel thicknessmayshed light on primate dental functional morphology and dietaryecology (e.g., Jolly, 1970; Gantt, 1977; Kay, 1981, 1985; Andrews andMartin, 1991; Dumont, 1995; Spears and Macho, 1998; Macho andSpears, 1999; Wrangham et al., 1999; Shimuzu, 2002; Martin et al.,2003; Kono, 2004; Grine et al., 2005; Teaford, 2007; Vogel et al.,2008; Lucas et al., 2008a, b; Constantino et al., 2009, 2011). Whilehominin dietary ecology remains a subject of great debate (e.g., Straitet al., 2009; Grine et al., 2010; Godfrey et al., 2011; Ungar andSponheimer, 2011), enamel thickness data from a temporallydiversehominin samplemayprovide insight intopotential ecologicaltransitions and the functional impact of routine tool use (Teaford,2007) or advances in food preparation (Wrangham et al., 1999).Moreover, studies of fossil hominins have largely been restricted tomolar enamel thickness (but see Beynon and Wood, 1986; Whiteet al., 1994, 2006), and it is unknown how other permanent teethcompare with the relatively thin-enameled chimpanzee dentition orthe thickly-enameled recent human dentition (Smith et al., 2008).For example, previous research suggested that Neanderthal anteriorteeth may have been adapted for frequent or heavy loading (Brace,1964; Antón, 1990), which is a potential correlate of thick enamel(Spears andMacho,1998;Macho and Spears,1999). If this is the case,Neanderthal anterior teeth may have thicker enamel than expected,based on extrapolations from molar teeth.

Hominin enamel thickness is most commonly assessed fromnaturally-fractured teeth, flat-plane radiographs, or low resolutionmedical tomography (Table 1), despite limitations inherent to eachof these methods that prohibit accurate characterization (reviewedin Olejniczak and Grine, 2006). More recently, micro-computedtomography (micro-CT) has been shown to yield accurateestimates of enamel thickness in fossil and recent taxa, and thistechnique can be performed non-destructively with industrialtomography systems or synchrotron X-ray micro-CT (Kono, 2004;Tafforeau, 2004; Olejniczak, 2006; Olejniczak and Grine, 2006;Smith et al., 2006b; Olejniczak et al., 2007; Kono and Suwa,2008). Here we apply micro-CT imaging to the largest sample ofhominin teeth studied to date to examine the taxonomic andfunctional signals of enamel thickness in a diverse global sample offossil Homo individuals. Specifically, we assess the taxonomic,geographic, and temporal trends in molar enamel thickness duringthe past two million years, which includes critical periods oftechnological development and widespread migration. We alsoprovide the first assessment of enamel thickness within entirehominin dentitions, focusing on Middle Paleolithic Homo species,which have been of considerable recent interest for taxonomic anddemographic assessments (Olejniczak et al., 2008a; Smith et al.,2009a; Bayle et al., 2010; Roksandic et al., 2011; Trinkaus, 2011;Benazzi et al., 2011a, b).

Methods

A total of 150 permanent fossil Homo teeth from a maximum of52 individuals were studied (Table 2, Appendix A). The samplespans approximately two million years of hominin evolution andincludes individuals from southern, eastern, and northern Africa,western and eastern Europe, Israel, mainland China, and Java. Thisstudy aims to compile all available standardized two-dimensional(2D) enamel thickness data for fossil Homo. To this end, valuesfrom 33 previously published molars were included, representing22% of the total sample (detailed in Appendix A). Isolated fossilteeth and those in situ were scanned with laboratory microtomo-graphic scanners (BIR Actis 300/225 FP or Skyscan 1172) with voxelsizes between 14 and 31 cubic micrometers, or with synchrotron

micro-CT on beamline ID19 of the European Synchrotron RadiationFacility (ESRF) with voxel sizes between 20 and 31 cubic microm-eters (as in Olejniczak et al., 2008a, b, d; Smith et al., 2009a, b,2010). We combined data from multiple imaging systems, asdifferent micro-CTs with similar scan parameters have been shownto yield relatively invariant enamel thickness measurements forteeth that have not been heavily remineralized (Olejniczak et al.,2007). Several of these scans are freely available in an open-access database administered by the ESRF (http://paleo.esrf.eu).

Although micro-CT imaging facilitates assessment of three-dimensional (3D) relative enamel thickness and tissue distribu-tion (e.g., Kono, 2004; Tafforeau, 2004; Smith et al., 2006b;Olejniczak et al., 2008a, b, d; Suwa et al., 2009), this approachrequires teeth that are essentially unworn and completely intact,which excludes most fossil hominin teeth. To maximize the use ofavailable samples, we assessed enamel thickness from virtual 2Dsection planes, which can be manually corrected for moderateattrition or tissue loss (detailed below). Section planes weregenerated from 3D models (interpolated image stacks made fromsuccessive cross-sectional slices output from tomographic recon-struction software) with VoxBlast Software (Vaytek, Inc.) or VGStudio MAX 2.0/2.1 (Volume Graphics, Inc.) (Supplementary Fig. 1).Virtual sectioning protocols have been published previously(Olejniczak, 2006; Feeney et al., 2010; Smith et al., 2010) and areonly briefly reviewed below.

For anterior teeth and premolars, 3D models were first orientedto view the occlusal surface (with the long axis of the tooth crownperpendicular to the plane of the computer screen). Incisors wereoriented with the incisal edge set horizontally and the widestlabial-lingual point set vertically. Subsequently, the dentine horntip of the central mammelon was located by virtually scrollingapically through the tooth image stack, and this point was set as thecenter of rotation. A 2D section was created for measurement byrotating the 3D model around this point to find the 2D labial-lingual plane that captured the widest bi-cervical diameter (andtypically the longest cervical enamel extension). Canine 3D modelswere virtually sectioned by orienting the maximum mesial-distalwidth of the crown vertically, and the dentine horn tip waslocated and set as the center of rotation (as for incisors). The finalsection plane was created by rotating the model to locate a labial-lingual plane that captured the maximum bi-cervical diameter(approximately perpendicular to the maximum mesial-distalwidth). For premolars, the buccal and lingual cusps of 3D modelswere aligned in a horizontal plane, and the dentine horn tip of thebuccal cusp was set as the center of rotation. To generate a buccal-lingual 2D section along the axis of the tooth, the model wasrotated to locate the plane midway between the maximum buccal-lingual bi-cervical diameter and the maximum cervical enamelextension (illustrated in Feeney et al., 2010: Fig. 1). Due to coronalasymmetry, Neanderthal lower fourth premolars were virtuallysectioned from the mesiobuccal to the distolingual cusp.

T.M. Smith et al. / Journal of Human Evolution 62 (2012) 395e411398

Virtual 2D molar sections were prepared following one of twomethods. The first method developed by Olejniczak (2006) involvesthree-dimensionally orienting an image stack parallel to a planedefined by three dentine horn tips (two mesial and one distal). Aperpendicular plane is then made through the dentine horn tips ofthe mesial cusps to yield a virtual 2D buccal-lingual section. Asecond method for cutting virtual molar 2D sections was recentlydetailed in Smith et al. (2010). Within the image stack, the 3Dcoordinates of the two dentine horn tips and two pulpal horn tips ofthe mesial cusps are found and recorded. The final 2D plane isdetermined from a midpoint between the two pulp chamber horntips and the two dentine horn tip coordinates using rotationalvectors with a dentine horn tip set as the center of rotation. Thismethod was designed to yield a 2D plane perpendicular to thedevelopmental axis of the crown that captures the maximumextension of the cervical enamel, as is standard practice for physicalsectioning (e.g., Smith et al., 2005). Data from both methods werecombined to maximize available fossil molar samples sincecomparisons of teeth cut with both methods did not revealsignificant differences in average or relative enamel thickness(Supplementary Methods).

A human comparative sample of 483 recent H. sapiens teeth wasalso employed (Smith et al., 2006a, 2008), which is based onphysical sections of unworn and lightly worn teeth cut in the sameplanes as the fossil sample. These preparative techniques arecomparable in principle; enamel thickness measurements takenfrom virtual and physical sections of the same samples have beenshown to differ by less than 5% (Tafforeau, 2004; Olejniczak andGrine, 2006). While imprecise physical sectioning can yield infla-ted enamel thickness values due to section obliquity (Martin, 1983;Smith et al., 2003; also see; Suwa and Kono, 2005), we tested this inthe carefully-sectioned teeth employed in this study by comparingmean linear enamel thickness values with virtual sections of otherrecent humans, and found no systemic bias (Smith et al., 2010).Enamel thickness variables were quantified on each 2D plane ofsection using a Wacom digitizing tablet and SigmaScan software(Systat Software, Inc.), or directly on digital images with ImageJsoftware (National Institutes of Health). Following Martin (1983),variables include the area of the enamel cap (c) in mm2, the lengthof the enamel-dentine junction (e) in mm, and the area of thecoronal dentine and pulp enclosed by the enamel cap (b) in mm2

(Supplementary Fig. 1). Slight reconstructions of the outer enamelsurfaceweremade prior tomeasurement for sections showing lightto moderate wear (based on the profiles of unworn teeth), or whena small amount of cervical enamel was missing (based on thecurvature and orientation of the outer enamel surface relative tothe enamel-dentine junction). When antimeres were available, the

Table 3Average enamel thickness (AET) values (in mm) in fossil and recent Homo molars.

Taxon Row M1 N MineMax

East African early Homo Max 1.20 1 e

South African early Homo e e e

Asian Homo erectus 1.20 2 1.17e1.23Archaic European Homo 1.08 1 e

Archaic North African Homo e e e

Homo neanderthalensis 1.06 9 0.95e1.19Fossil Homo sapiens 1.28 4 1.08e1.58Recent Homo sapiens 1.22 40 0.98e1.50

East African early Homo Mand 1.47 1 e

South African early Homo 1.77 2 1.76e1.77Archaic European Homo e e e

Homo neanderthalensis 1.00 13 0.90e1.18Fossil Homo sapiens 1.19 6 0.96e1.47Recent Homo sapiens 1.08 58 0.80e1.40

Row: Max ¼ maxillary molars, Mand ¼ mandibular molars. M1: first molar mean AET; M

side with the lowest relative enamel thickness was used (followingMartin, 1983). Teeth that had yet to finish crown formation, or weremissing both cervices, were not employed in this study.

Average enamel thickness (AET) is calculated as [c/e], yieldingthe mean straight-line distance (in mm) from the enamel-dentinejunction to the outer enamel surface. Relative enamel thickness(RET) is calculated as [100 * AET/Ob]. This is a unitless measurewherein AET is scaled for size, yielding a measurement suitable forinter-taxon comparisons (Martin, 1983, 1985). The RET index wasoriginally developed by Martin (1983) for comparisons of primatemolars among species with different body sizes, rather thancomparisons within individuals or taxonomic groups. We haveincluded RET here in addition to the AET index since tooth size hasdecreased throughout the evolution of Homo, and body mass hasfluctuated as well (Brace et al., 1987; Ruff, 2002; Lieberman, 2011)(discussed further in Supplementary Methods). Statistical testswere performed with SPSS software (v. 18, IBM Corp.), and includenon-parametric ManneWhitney U tests for comparisons betweentaxa for tooth positions represented by four or more elements.

Results

Molar enamel thickness in fossil Homo

Average and relative enamel thickness (AET and RET) values forthe molar sample are given in Tables 3 and 4. Average enamelthickness values for the fossil Homo sample range from 0.90 to2.20 mm (n ¼ 81 teeth), and the recent H. sapiens sample rangesfrom 0.80 to 1.95mm (n¼ 271 teeth). FossilHomomolar RET valuesfall between 12.7 and 29.5, while recent H. sapiens values fallbetween 11.8 and 31.8. Given that enamel thickness varies amongtooth positions, increasing throughout the molar row (Smith et al.,2005, 2006a, 2008; Grine, 2005a), subsequent comparisons amonggroups are made within tooth positions. Neanderthal first molars(M1s) show the thinnest average and relative enamel thickness.Low values are also seen in archaic European maxillary M1 AET aswell as for RET in small samples of archaic European Homo andearly Homo from east Africa and Asia, respectively. In contrast, twomandibular M1s and one maxillary M2 from South African earlyHomo show the thickest average and relative enamel of the fossilsample, greatly exceeding respective recent human values. TwoM2s from east Africa also show exceptionally thick enamel, fallingnear or above recent human AET maxima. Third molars are repre-sented by fewer taxa, with Neanderthals again showing the lowestAET and RET values. Due to limited sample sizes, statisticalcomparisons of enamel thickness and its components are onlypossible among Neanderthal, fossil H. sapiens, and recent H. sapiens

M2 N MineMax M3 N MineMax

1.69 1 e e e

2.20 1 e e e

1.48 1 e 1.33 3 1.13e1.511.20 1 e 1.25 1 e

1.42 1 e 1.56 1 e

1.17 6 1.09e1.29 1.22 5 1.11e1.351.31 1 e e e e

1.40 29 1.13e1.84 1.38 52 1.18e1.95

1.72 1 e e e e

e e e e e e

e e e 1.27 1 e

1.03 6 0.96e1.08 1.01 6 0.91e1.161.28 4 1.17e1.41 1.28 2 1.15e1.411.20 47 0.94e1.55 1.25 45 0.98e1.74

2: second molar mean AET; M3: third molar mean AET.

Table 4Relative enamel thickness (RET) values in fossil and recent Homo molars.

Taxon Row M1 N MineMax M2 N MineMax M3 N MineMax

East African early Homo Max 15.6 1 e 18.7 1 e e e

South African early Homo e e e 29.5 1 e e e

Asian Homo erectus 15.8 2 15.3e16.3 19.4 1 e 20.2 3 18.7e22.5Archaic European Homo 16.9 1 e 17.1 1 e 21.6 1 e

Archaic North African Homo e e e 18.8 1 e 22.9 1 e

Homo neanderthalensis 15.3 9 13.1e16.9 17.1 6 14.9e19.5 18.1 5 16.4e20.9Fossil Homo sapiens 18.2 4 15.7e20.9 19.8 1 e e e e

Recent Homo sapiens 18.7 40 14.0e23.9 21.4 29 16.5e28.0 21.8 52 17.0e30.0

East African early Homo Mand 21.5 1 e 26.2 1 e e e e

South African early Homo 29.0 2 28.7e29.3 e e e e e e

Archaic European Homo e e e e e e 21.5 1 e

Homo neanderthalensis 15.4 13 12.7e20.5 15.5 6 13.9e16.5 16.8 6 14.3e18.3Fossil Homo sapiens 18.0 6 15.2e23.3 18.3 4 16.3e20.2 20.5 2 19.2e21.9Recent Homo sapiens 17.0 58 11.8e22.6 20.5 47 14.8e27.7 21.7 45 17.2e31.8

Row: Max ¼ maxillary molars, Mand ¼ mandibular molars. M1: first molar mean RET (dimensionless unit); M2: second molar mean RET; M3: third molar mean RET.

T.M. Smith et al. / Journal of Human Evolution 62 (2012) 395e411 399

molars. Neanderthal AET and RET molar values are significantlylower than recent humans, which is largely due to greater enamel-dentine junction lengths and dentine areas in the former taxon(Table 5). Neanderthals also typically show significantly lower AETand RET values when compared with fossil H. sapiens M1s andmandibular M2s (Table 6), although differences between mandib-ular M1 RET values approach but do not achieve significance. Thesedifferences appear to be due to lower enamel cap areas in Nean-derthals than in fossil H. sapiens. Finally, comparisons betweenrecent and fossil H. sapiens did not reveal differences in AET or RET,although enamel cap area, enamel-dentine junction lengths, anddentine areaswere generally significantly greater in fossilH. sapiens(Table 7).

Few temporal or geographic trends in enamel thickness areevident (Fig. 1). Early Homo molars from east Africa, South Africa,and Asia show a wide range of AET and RET values. Archaic Euro-pean Homo (Steinheim and Mauer) values show a mixed pattern;maxillary AET values from Steinheim are comparable to Neander-thal means, while the Mauer mandibular M3 AET value exceeds thesix Neanderthal mandibular M3s. Relative enamel thickness values

Table 5ManneWhitney U test for differences in the components of enamel thicknessbetween Neanderthals and recent humans.

Tooth Statistic c e AET b RET

UI1 Z �0.977 �1.955 �0.400 �3.288 �2.577p 0.328 0.051 0.689 0.001 0.010

UI2 Z �3.133 �3.225 �1.715 �3.408 �2.447p 0.002 0.001 0.086 0.001 0.014

UC Z �1.066 �2.487 �1.492 �2.772 �2.985p 0.286 0.013 0.136 0.006 0.003

UP4 Z �0.244 �2.257 �1.891 �2.562 �3.050p 0.807 0.024 0.059 0.010 0.002

UM1 Z �0.981 �3.667 �3.255 �2.530 �3.925p 0.327 <0.001 0.001 0.011 <0.001

UM2 Z �1.401 �1.926 �3.240 �1.094 �3.151p 0.161 0.054 0.001 0.274 0.002

UM3 Z �0.705 �2.059 �2.288 �1.410 �2.821p 0.481 0.039 0.022 0.158 0.005

LM1 Z �0.282 �2.795 �2.082 �1.472 �2.349p 0.778 0.005 0.037 0.141 0.019

LM2 Z �0.786 �2.218 �3.117 �3.116 �3.734p 0.432 0.027 0.002 0.002 <0.001

LM3 Z �2.310 �0.614 �3.276 �0.994 �3.801p 0.021 0.539 0.001 0.320 <0.001

Tooth: U emaxillary, L emandibular; c: area of the enamel cap; e: enamel-dentinejunction length; AET: average enamel thickness; b: area of coronal dentine; RET:relative enamel thickness. Significant differences (p< 0.05) are in bold. Comparisonswere not made for tooth positions represented by less than four teeth.

of archaic European Homo molars exceed Homo neanderthalensisand are more similar to other later Homo taxa, save for the lonemaxillary M2 value from Steinheim, which is equivalent to theNeanderthal mean value. Differences in these two indices are due inpart to greater dentine areas in Neanderthal molars. When onlylater Homo species are considered (including archaic groups),archaic North African Homo and fossil H. sapiens show the highestmolar AET values, and recent H. sapiens show the highest mean RETwithin four of 6 M positions (archaic North African Homo and fossilH. sapiens show the highest values for the other two positions).

Enamel thickness in full dentitions of fossil Homo

Mean values of enamel thickness indices and their componentsare given for all available tooth positions in Appendix B. Early Homocanine and premolar teeth, derived from six individuals from Asiaand Africa, show substantial variation. The AET value of themaxillary canine of KNM-ER 1590 falls at the low end of recenthuman ranges (and the RET value falls below recent human rangesdue to its massive dentine area) while the mandibular thirdpremolars (P3s) of KNM-ER 1802 and a Chinese H. erectus indi-vidual are near or beyond recent human AET and RET rangemaxima. Similarly, the maxillary P3 AET and RET values of theSouth African specimen SK 27 fall beyond or at the high end ofrecent human ranges, respectively. Trends in later Homo anteriorteeth and premolar AET and RET largely parallel those in molarenamel thickness. The maxillary P4 AET and RET values of onearchaic European Homo individual are similar to recent humans,while the maxillary premolars of one archaic northern AfricanHomo show high AET values, but RET values that are also similarto recent humans. Figs. 2 and 3 compare Neanderthal, recentH. sapiens, and fossil H. sapiens full dentition AET and RET values(other taxa are excluded for clarity). While incisor AET is fairly

Table 6ManneWhitney U test for differences in the components of enamel thicknessbetween Neanderthals and fossil H. sapiens.

Tooth Statistic c e AET b RET

UM1 Z �1.543 �0.617 �2.315 �0.617 �2.315p 0.123 0.537 0.021 0.537 0.021

LM1 Z �2.193 �0.175 �2.105 �0.263 �1.842p 0.028 0.861 0.035 0.792 0.066

LM2 Z �2.345 �0.640 �2.558 �1.066 �2.345p 0.019 0.522 0.011 0.286 0.019

Significant p-values are in bold. Comparisons were not made for tooth positionsrepresented by less than four teeth.

Table 7ManneWhitney U test for differences in the components of enamel thicknessbetween fossil H. sapiens and recent humans.

Tooth Statistic c e AET b RET

UM1 Z �1.674 �2.287 �0.409 �2.164 �0.572p 0.094 0.022 0.683 0.030 0.568

LM1 Z �2.027 �2.660 �1.187 �0.806 �0.576p 0.043 0.008 0.235 0.420 0.565

LM2 Z �2.838 �3.048 �1.297 �3.224 �1.647p 0.005 0.002 0.195 0.001 0.100

Significant p-values are in bold. Comparisons were not made for tooth positionsrepresented by less than four teeth.

T.M. Smith et al. / Journal of Human Evolution 62 (2012) 395e411400

invariant among taxa, Neanderthals show the lowest median AETvalues for canines, premolars, and molars. Fossil and recentH. sapiens AET values are broadly comparable, save for high AETvalues in maxillary premolars of the former taxon. Relative enamelthickness values across the dentition tend to be lowest in Nean-derthals and greatest in recent H. sapiens (Fig. 3). Differencesbetween Neanderthals and recent H. sapiens RET are significant foreach tooth position represented by four or more elements,including the maxillary incisors, canine, fourth premolars, andmolars (Table 5). While samples of fossil H. sapiens anterior teeth,premolars, and certain molar positions are insufficient for statis-tical comparisons, RET values tend to fall between those of Nean-derthals and recent humans.

In order to discern underlying causes of AET and RET variationamong Neanderthals and recent and fossil H. sapiens, we examinedenamel cap area and dentine area. Trends in enamel cap area arecomplex. Neanderthals show the greatest values for maxillarylateral incisors (I2) and canines, as well as mandibular incisors(Fig. 4). Differences between Neanderthals and recent humanmaxillary I2s are significant (Table 5). Postcanine enamel cap area istypically greatest in fossil H. sapiens, and comparable in Neander-thals and recent humans. Consideration of dentine area revealsparticularly marked differences. Neanderthals generally have thegreatest dentine areas for most maxillary teeth and the mandibularincisors, while fossil H. sapiens have the highest dentine areas forthe rest of the mandibular dentition (Fig. 5). Differences in dentinearea between Neanderthal and recent H. sapiens are significant formost maxillary teeth (Table 5). In summary, Neanderthal canine,premolar andmolar teeth typically show lower average and relativeenamel thickness values due to markedly greater dentine areas(and enamel-dentine junction lengths) than in recent humans.Values for Neanderthal incisor AET seem to depart from this trend;these are broadly comparable among all three taxa, which is due tosimilarities in the proportions of enamel cap area and enamel-dentine junction lengths within each group. Although fossil andrecent H. sapiens show broadly similar AET values, recent H. sapiensshow relatively thicker enamel due to substantial reduction indentine area accompanied by only minor reduction in enamel area.Sample sizes of fossil H. sapiens anterior teeth and premolars weretoo small to assess this statistically.

Discussion

Variation in hominin and hominoid enamel thickness

Examination of AET and RET in the permanent dentition of fossilHomo reveals variation within both geologically older taxa (>onemillion years old: east and South African early Homo, AsianH. erectus from Sangiran (Antón, 2003)) and younger taxa (<onemillion years old: the remainder of the sample). Variation in AETand RET is also substantial within African, Asian, and Europeanfossil groups, which is consistent with population-level variation in

recent H. sapiens (Smith et al., 2006a; Feeney et al., 2010). In thefollowing sections, we focus on the taxa showing the highest andlowest AET and RET values, followed by a consideration of trends inthe dental tissue proportions that make up these indices.

A particularly surprising finding is that AET and RET values inthe two early Homo mandibular M1s from Drimolen, South Africa(DNH 35 and 67) are closer to those of Paranthropus robustus M1s(AET: 1.55e2.03 mm; RET: 25.0e30.5, n ¼ 2: Olejniczak et al.,2008b) than to other fossil Homo or recent H. sapiens. Three linesof evidence suggest that these ‘hyper-thick-enameled’ teeth belongtoHomo. The DNH 35M1 is part of a mandibular dentitionwith firstand second deciduous molars. The morphology and metricalfeatures of each of these teeth are quite distinct from Paranthropusmolars, and for this reason it has been attributed to Homo (Keyseret al., 2000). The specimen DNH 67 was provisionally attributedto P. robustus (Keyser et al., 2000) but its taxonomic affiliation hassince been revised to ‘Homo?’ (Moggi-Cecchi et al., 2010), anda recent developmental study demonstrated that DNH 67 belongsto the same individual as DNH 70 and 71 (both independentlyattributed to Homo sp. by Moggi-Cecchi et al., 2010) as all threeteeth show identical internal stress patterns (Tafforeau et al., 2011).Finally, a similar high RET value (29.5) was found for the maxillarysecond molar from Swartkrans (SK 27), which is in a juvenilecranium that shows similarities to other early Homo (Clarke, 1977;Grine, 2005b). By employing medical computed tomography,Schwartz (1997) first reported that SK 27 showed extremely thickmolar enamel, similar to the Paranthropus condition. He also notedthat the SK 268 early Homo molar did not show extremely thickenamel, resembling the ‘thick’ condition of Australopithecus afri-canus and recent humans. We concur with these characterizations,although we are unable to quantify RET in SK 268 as it has beenphysically sectioned through the mesial cusps (and is fractured),prohibiting virtual sectioning with the protocol described above.

The current studyalso demonstrates thatNeanderthal dentitionstypically have thinner enamel than recent H. sapiens due to differ-ences in dental tissue proportions, as has been previously reportedfor permanent molar teeth (Olejniczak et al., 2008a; Bayle et al.,2010; Kupczik and Hublin, 2010). Moreover, our data reveal thefirst significant differences in AET and RET between Neanderthalsand fossil H. sapiens for certain molar positions. These findings arebroadly consistent with comparisons of dental tissue proportions indeciduous teeth fromNeanderthals and Upper PaleolithicH. sapiens(Bayle et al., 2009a, b, 2010; Benazzi et al., 2011a). Neanderthals alsoappear to have relatively thinner enamel than earlier archaic Homo,aswell as afirstmolar ofHomoantecessor (Bermúdezde Castro et al.,2010: Fig. 1). While it is tempting to suggest that absolutely andrelatively thin enamel may be a derived trait in Neanderthals,evidence from an expanded sample of archaic Homowould providemore insight into this unusual hominin condition.

We have also demonstrated that recent humans have relativelythicker enamel than fossil H. sapiens across the complete dentition,although AET values are more similar. Differences in RET areprimarily due to smaller coronal dentine areas in recent humans(enamel cap area is often lower as well). In contrast to increasingtrends in brain and body mass during the Paleolithic, hominindentitions decreased in size (Brace et al., 1987, 1991), which somehave suggestedwas due to advances in food preparative techniques(Brace, 1964; Brace and Ryan, 1980; Brace et al., 1987, 1991;Franciscus and Trinkaus, 1995). It is unclear why crown sizereduction from fossil H. sapiens to recent humans resulted froma proportionately greater reduction in coronal dentine than enamel.Tooth root volumes and jaw size have also reduced considerablyduring the Paleolithic (Kupczik and Hublin, 2010; Lieberman, 2011),and it appears that enamel volume is regulated, in part, by inde-pendent mechanisms. There are numerous similarities between

Figure 1. Relative enamel thickness in fossil and recent Homo molars. Groups are arranged in approximate chronological order from geologically oldest (left) to youngest (right).Standard box and whisker plot revealing the interquartile range (25the75th percentiles: boxes), 1.5 interquartile ranges (whiskers) and the median values (black line). Outliers morethan 1.5 interquartile ranges from the box are signified with circles.

T.M. Smith et al. / Journal of Human Evolution 62 (2012) 395e411 401

Figure 2. Average enamel thickness (in mm) in Neanderthal, fossil H. sapiens, and recent H. sapiens full dentitions. See Fig. 1 for explanation of graphs.

T.M. Smith et al. / Journal of Human Evolution 62 (2012) 395e411402

Figure 3. Relative enamel thickness in Neanderthal, fossil H. sapiens, and recent H. sapiens full dentitions. See Fig. 1 for explanation of graphs.

T.M. Smith et al. / Journal of Human Evolution 62 (2012) 395e411 403

Figure 4. Enamel cap area (in mm2) in Neanderthal, fossil H. sapiens, and recent H. sapiens full dentitions. See Fig. 1 for explanation of graphs.

T.M. Smith et al. / Journal of Human Evolution 62 (2012) 395e411404

Figure 5. Dentine area (in mm2) in Neanderthal, fossil H. sapiens, and recent H. sapiens full dentitions. See Fig. 1 for explanation of graphs.

T.M. Smith et al. / Journal of Human Evolution 62 (2012) 395e411 405

T.M. Smith et al. / Journal of Human Evolution 62 (2012) 395e411406

dentine and bone that are not shared with enamel, particularly intheir embryonic origins, responsiveness to specific developmentalsignaling molecules, retention of formative cells with network-likeconnections throughout life, organic composition, and degree ofmineralization (e.g., MacDougall et al., 2006; Lu et al., 2007; Qinet al., 2007; Sun et al., 2011). Irrespective of the etiology of differ-ences in dental tissue proportions, it appears that relatively thickenamel in recent human is achieved through a different develop-mental mechanism than in earlier thick-enameled hominins (alsosee Grine, 2002, 2005a), further confirming that it is not a usefulcharacter for assessments of hominin phylogeny. This is also sup-ported by reports that fine-scaled developmental mechanisms suchas cuspal enamel secretion rates may vary among hominins withsimilar degrees of absolutely and relatively thick enamel (Deanet al., 2001; Lacruz et al., 2008).

Beyond the inherent difficulties of assessing a highly variabletrait in small fossil samples, elucidating the underlying causes ofenamel thickness variation is also complicated by the lack ofinformation on AET or RET in species of earlier hominins or extanthominoids. Suwa et al. (2009) contrast maximum lateral enamelthickness (linear values measured from naturally-fractured teeth ormicro-CT scans) in species of Pan and Australopithecus. While valuesfrom the two chimpanzee species are similar, lateral enamelthickness appears to increase about 20% from Australopithecusanamensis to Australopithecus afarensis to A. africanus, althoughassessment of these trends is complicated by a lack of informationon tooth and cusp types. The only hominoid known to showa degree of interspecific RET variation comparable with Homo is theearly Miocene genus Proconsul, which ranges from thin enamel inProconsul africanus to thick enamel in Proconsul nyanzae (reviewedin Smith et al., 2006a). However, Proconsul shows markedly greatervariation in body mass and presumptive ecological niches thanHomo, spanned a longer geological period, and is considered bysome to include species that belong in a separate genus (e.g., Begun,2007).

Broader implications of enamel thickness studies

In the following sections, we discuss the broader implications ofour results for studies of hominin taxonomy, functionalmorphology,and paleodemography. The current study demonstrates that thetaxonomic utility of AET and RET is rather limited, particularly forcomparisons of small early hominin samples. When both recent andfossilHomomolars are combined, certainpositions show substantialoverlap with A. africanus and P. robustus (Olejniczak et al., 2008b).WhilemeanRET values in fossil hominins are unlikely to be as lowasthose of living African apes, the often-cited dichotomy of thickversus thin enamel in these groups is an oversimplification. Aminordegree of overlap in molar RET is also evident among Neanderthals,recent humans, and African apes, although significant differencesare apparent (Smith et al., 2008; this study). Similarly, while linearenamel thickness values in Ardipithecus ramidus are somewhatgreater than those of chimpanzees, overlap has also been reported(White et al., 1994; Suwa et al., 2009). Thus congeneric variationdocumented in the current study lends support to the argument byHaile-Selassie et al. (2004) that reported enamel thickness variationin Sahelanthropus, Orrorin, and Ardipithecus does not necessarilysupport their generic distinction.

Several recent studies have documented enamel thickness inEuropean Middle Paleolithic Homo (Olejniczak et al., 2008a; Smithet al., 2009a; Bayle et al., 2010; Roksandic et al., 2011; Benazziet al., 2011a, b), as the absolutely and relatively thin enamel ofNeanderthals may facilitate taxonomic discrimination with respectto H. sapiens. Both 2D and 3D assessments have confirmed thatsignificant differences exist between these taxa, although the

current study suggests that RET differences across the dentition areless pronounced between Neanderthals and fossil H. sapiens thanbetween Neanderthals and recent H. sapiens. However, additionalstudy is required to assess the degree of overlap, as our sample isbased exclusively on African and Middle Eastern fossil H. sapiens.Bayle et al. (2009a, 2010) examined 3D enamel thickness in theprimarily deciduous dentitions of two Upper Paleolithic Europeanchildren, and found greater similarities with recent humans thanwith Neanderthals (particularly for AET), although samples weretoo small for statistical assessment. Benazzi et al. (2011a) alsocompared small samples of Neanderthal, Upper PaleolithicH. sapiens and recent human deciduous molars, finding greater AETandRETvalues in fossilH. sapiens than in recentH. sapiens (both taxawere thicker than Neanderthals). Future taxonomic studies ofhominin dental remainsmayalso benefit frommore comprehensiveassessments of internal and external crown and root structure (e.g.,Skinner et al., 2009; Smith et al., 2009b; Kupczik and Hublin, 2010;Benazzi et al., 2011b), which may be coupled with information onhard tissue development (Beynon and Wood, 1986; Dean et al.,2001; Lacruz et al., 2008; Smith et al., 2009a; Bayle et al., 2010).

The adaptive significance of hominin enamel thickness alsoremains elusive, as it does not appear that increased reliance ontool use has led to decreased enamel thickness during theevolution of Homo (contra Teaford, 2007), although we note thatseveral early Homo individuals do show extremely thick enamel.Similarly, there is little evidence to suggest that increasingsophistication in food preparation has resulted in thinner enamelin most later Homo species (contra Wrangham et al., 1999). It isperhaps less clear if potentially increased anterior tooth use inNeanderthals (Brace, 1964; Antón, 1990) led to thicker enamel,which has been posited as an adaptive response to increased orsustained loading (Spears and Macho, 1998; Macho and Spears,1999). In contrast with the rest of the dentition, Neanderthalincisors have average enamel thickness values that are similar tofossil and recent H. sapiens. These teeth, which are known to belarge relative to the rest of the dentition (Wolpoff, 1979) arecharacterized by large dentine areas, as well as large enamel capareas (significantly greater than recent humans for maxillary I2s).A similar but more marked trend is found when orangutan inci-sors are compared with other great ape incisors (Smith, unpub-lished data), which may relate to bark gouging or incisal bitingof mechanically demanding foods (Rodman, 1988; Taylor, 2006),a behavior that is uncommon in other great apes. Furthercomparative study is needed to assess enamel thickness anddental tissue proportions in other primates that employ theiranterior dentition for processing mechanically demanding foods(Ungar, 1994; Martin et al., 2003).

Grine (2005a) reviewed evidence for the functional signifi-cance of recent human enamel thickness, which he regarded asequivocal given the lack of concordance between molar biteforces and enamel thickness patterning. Molar bite force isgreatest at the first molar and decreases toward the third molar,yet enamel thickness increases from first to third molars. It isimportant to note that thick molar enamel is not a prerequisite forhard-object feeding, as pithiciin primates use their anterior teethto open hard outer shells while pulping soft and elastic seedswith their thin-enameled molars (Martin et al., 2003). Sea otters,which are known to routinely consume extremely hard marineinvertebrates, have also been reported to have thin enamel(Constantino et al., 2011). Moreover, Dumont (1995) concludedthat there does not appear to be a particular relative enamelthickness threshold that distinguishes hard- and soft-objectfeeders, and that dietary inferences based on enamel thicknessalone should be treated with caution. While current biomechan-ical models postulate that thick enamel may serve to resist

Fossil Homo dental material included in this study.

Sample Site Individual N Source

East Africanearly Homo

Koobi Fora, Kenya KNM-ER 1590 5 1Koobi Fora, Kenya KNM-ER 1802 4 1

South Africanearly Homo

Drimolen, South Africa DNH 35 1 1Drimolen, South Africa DNH 67a 1 1Swartkrans,South Africa

SK 27 2 1

AsianHomo erectus

Trinil, Java 11620 1 2China(Apothecary Collection)

CA 770 1 1

China(Apothecary Collection)

CA 771 1 1

Sangiran, Java S7-4 4 1Zhoukoudian, China M3549 1 1Zhoukoudian, China M3550 1 1Zhoukoudian, China M3887 1 1

(continued on next page)

T.M. Smith et al. / Journal of Human Evolution 62 (2012) 395e411 407

abrasion and/or fracture (Lucas et al., 2008a, b), primates andother mammals may employ complementary methods for pro-cessing hard and/or abrasive foods, such as anterior tooth pro-cessing (Ungar, 1994; Martin et al., 2003), washing sandy fooditems before consumption (Visalberghi and Fragaszy, 1990), oremploying tools to crack open hard food items (Hall and Schaller,1964; Fragaszy et al., 2004), leading to thinner enamel than ex-pected in certain instances (Martin et al., 2003; Constantino et al.,2011). In addition to the challenge of distinguishing the adaptivesignificance of thick enamel for resisting either abrasion or frac-ture (which may result from disparate diets but lead to conver-gent morphologies), dietary assessments from enamel thicknessvalues may be further complicated by non-masticatory behaviors,which may bias these predictions under certain conditions.

Our results support previous research demonstrating thatwhole-crown 3D enamel thickness is variable within hominins andamong other primate clades (Kono, 2004; Olejniczak et al., 2008a,b, d). In light of such variation in whole-crown metrics, severalstudies have suggested that tooth function may be better under-stood in terms of the 3D distribution of enamel across the entiremolar crown (Kono, 2004; Tafforeau, 2004; Olejniczak et al., 2008a,b, d; Suwa et al., 2009) rather than from enamel thickness indicessummarizing a single plane of section or the entire tooth. To thisend, recent innovative micro-CT studies of hominin and hominoidmolars have virtually separated enamel in the occlusal basinfrom the lateral walls (Kono and Suwa, 2008; Suwa et al., 2009).Comparisons of whole-crown, lateral, and occlusal thickness havedemonstrated that Pan and Gorilla molars have different enameldistribution patterns despite broadly similar RET values. Impor-tantly, these authors argued that differences in enamel thicknessdistribution may be partially explained by differing functionaladaptations in the two groups. Soft-fruit consumption in Pan maybe related to their thinner occlusal enamel, as this unique pattern isalso observed in a frugivorous Hylobates lar molar, in contrast withGorilla, Homo, and Pongo, which are characterized by a relativelythicker occlusal basin compared with the lateral molar walls.Others have also demonstrated that broadly similar 3D molar RETvalues in A. africanus and H. sapiens (Olejniczak et al., 2008b), andPongo pygmaeus and Gigantopithecus blacki (Olejniczak et al.,2008c) are accompanied by different patterns of 3D enameldistribution in these pairs, confirming that whole-crown 3Denamel thickness indices do not necessarily reflect the functionaldemands of molars. More nuanced interpretations of the functionalsignificance of enamel thickness may require integrating quanti-tative 3D enamel thickness assessments (Kono, 2004; Tafforeau,2004; Olejniczak et al., 2008a, b, c, d; Suwa et al., 2009), biome-chanics of the craniofacial complex (Grine et al., 2005; Strait et al.,2009; Berthaume et al., 2010; Wroe et al., 2010), and/or consider-ations of the material properties of dietary items and tooth enamel(Macho and Spears, 1999; Vogel et al., 2008; Lucas et al., 2008b; Leeet al., 2010).

Finally, our results have important implications for studies ofdental attrition and paleodemography in fossil hominins. Trinkaus(2011) recently argued that Neanderthals and fossil H. sapiensshow similar mortality patterns based on relative age categoriesdelineated from wear stages of postcanine teeth. However, Nean-derthal postcanine teeth have absolutely thinner enamel than fossiland recent H. sapiens (Fig. 2, Tables 5 and 6; also see linear enamelthickness data in Smith et al., 2010). This difference biasescomparisons, as Neanderthal postcanine teeth would appear moreworn (have more exposed dentine) than those of similarly-agedfossil H. sapiens, assuming similar diets and/or equal rates ofattrition. It is tempting to relate the thin enamel of Neanderthalmolars to evidence that northern and central Europe populationsincorporated a high proportion of meat in their diets (Richards

and Trinkaus, 2009; El Zaatari et al., 2011), as highly carnivorousmammals show thinner enamel than herbivorous mammals(Mackiewicz et al., 2010). Upper Paleolithic hominins appear tohave exploited a more diverse diet (Richards and Trinkaus, 2009),although it is highly likely that local ecological conditions affectedthe diets of both groups (Fiorenza et al., 2011). Recent evidence fromdental attrition and calculus analysis suggests that Neanderthalsalso incorporated plant material in their diets, particularly in moreforested or temperate climates (El Zaatari et al., 2011; Fiorenza et al.,2011; Henry et al., 2011). This may represent an additional source ofvariation in attrition rates. Another plausible source of bias may bedue to variation in eruption ages between Neanderthals and fossilH. sapiens, which appear to differ for postcanine teeth (Smith et al.,2007). Given themarked enamel thickness variation documented inthe current study, as well as potential dietary and developmentaldifferences between these groups (Richards and Trinkaus, 2009;Smith et al., 2010; Fiorenza et al., 2011), demographic profilesattained from dental attrition patterns that employ intra-taxonseriation (Caspari and Lee, 2004) are likely to be more accuratethan age estimates derived from standard wear stages (Trinkaus,2011).

Acknowledgments

We gratefully acknowledge Heiko Temming, Andreas Winzer,Diana Carstens, Cornelia Schicke, Silke Streiber, Adeline Le Cabec,Joane Pouech, Alexandra Houssaye, Daniel Green, Sophie Sanchez,Per Ahlberg, the National Museum of Kenya, the NESPOS Society,and the beamline ID 19 staff for assistance with obtaining micro-CTdata. Per Ahlberg, Mohamed Boutakiout, Jan Ove Ebbestad, MatsEriksson, Fred Grine, Assaf Marom, David Morris, EmmaMbua, YoelRak, Jean-Paul Raynal, Antonio Rosas, Catherine Schwab, FrancisThackeray, John de Vos, Reinhard Ziegler, and Bernhard Zipfelkindly provided specimen access, and Kornelius Kupczik assistedwith figure preparation. David Begun and several anonymousreviewers provided helpful comments on this manuscript. Thisstudy was funded by the Max Planck Society, the EuropeanSynchrotron Radiation Facility, Harvard University, EVAN MarieCurie Research Training Network grant MRTN-CT-019564 to theMax Planck Society, and the South African National ResearchFoundation (African Origin Platform, grant number 65155).

Appendix. Supplementary material

Supplementary data related to this article can be found online atdoi:10.1016/j.jhevol.2011.12.004.

Appendix A

Appendix A (continued )

Sample Site Individual N Source

ArchaicEuropean Homo

Heidelberg, Germany Mauer 1 1Steinheim, Germany Steinheim 4 1

ArchaicNorth African Homo

Thomas Quarry 1,Morocco

Thomas Quarry 1 1 3

Thomas Quarry 3,Morocco

Thomas Quarry 3 4 1

Homoneanderthalensis

Engis, Belgium Engis 2 2 1Abri Bourgeois-Delaunay, France

BD01 1 4

Abri Bourgeois-Delaunay, France

BD-J4-C9 1 4

Ehringsdorf,Germany

EhringsdorfG-1048-69

1 4

Devil’s Tower,Gibraltar

Gibraltar 2 6 1

Krapina, Croatia Krapina Maxilla B 5 1Krapina, Croatia Krapina Maxilla C 3 1Krapina, Croatia K10 1 4Krapina, Croatia K45 1 4Krapina, Croatia K6 1 4La Quina, France La Quina H18 6 1La Quina, France La Quina Q760-H9 2 1,4Le Moustier, France Le Moustier 1 16 1Regourdou, France Regourdou 1 2 4Roc de Marsal, France Roc de Marsal 1 4Scaldina Cave, Belgium Scladina 13 1Abri Suard, France S14-7 1 4Abri Suard, France S43 1 4Abri Suard, France S36 2 4Abri Suard, France S5 1 4Abri Suard, France S49 1 4El Sidron, Spain Juvenile (SD-531) 1 4El Sidron, Spain Adolescent 1 (SD-755) 1 4El Sidron, Spain Adolescent 2 (SD-540,

551, 621, 741, 1105)5 4

El Sidron, Spain Adolescent 3(SD-4, SD-332)

2 4

El Sidron, Spain Adult 6 (SD-407) 1 4Fossil Homo sapiens Dar es Soltane II,

MoroccoDar es Soltan II-4 3 1

Equus Cave,South Africa

EQ (H5) 1 5

Grotte desContrebandiers,Morocco

H7 1 6

Jebel Irhoud,Morocco

Irhoud 3 5 1

Jebel Qafzeh, Israel Qafzeh 10 8 1Jebel Qafzeh, Israel Qafzeh 15 13 1Die Kelders Cave,South Africa

SAM-AP 6242 1 5

Die Kelders Cave,South Africa

SAM-AP 6277 1 5

Grotte desContrebandiers, Morocco

T3b 1 6

Grotte desContrebandiers, Morocco

‘Temara mandible’ 5 1

Total 150

a See text for a discussion of the reclassification of this tooth. Source: 1 e this study; 2e Smith et al., 2009b; 3 e Raynal et al., 2010; 4 e Olejniczak et al., 2008a; 5 e Smithet al., 2006b; 6 e Hublin et al., in press.

Appendix B (continued )

Sample Tooth N c e AET b RET

LP3 1 30.54 20.03 1.52 43.05 23.23LP4 1 31.65 19.63 1.61 38.70 25.92LM1 1 30.72 20.85 1.47 46.98 21.50LM2 1 34.58 20.06 1.72 43.37 26.18

South African early Homo UP3 1 40.96 24.97 1.64 63.26 20.62UM2 1 49.58 22.49 2.20 55.84 29.50LM1 2 33.78 19.18 1.77 36.97 28.98

Asian early Homo UP3 1 24.74 20.72 1.19 46.38 17.53UP4 1 22.69 20.80 1.09 42.93 16.65UM1 2 30.04 25.01 1.20 57.82 15.80UM2 1 33.73 22.86 1.48 57.70 19.42UM3 3 26.84 20.01 1.33 43.79 20.21LP3 1 17.79 15.13 1.18 25.51 23.29LP4 1 21.76 19.98 1.09 36.80 17.96

Archaic European Homo UP4 1 23.46 20.66 1.14 40.33 17.88UM1 1 23.25 21.49 1.08 40.99 16.90UM2 1 25.79 21.51 1.20 48.99 17.13UM3 1 22.02 17.66 1.25 33.35 21.59LM3 1 24.05 18.98 1.27 34.58 21.55

Archaic NorthAfrican Homo

UP3 2 28.05 22.59 1.24 55.94 16.50UP4 1 29.69 22.51 1.32 54.25 17.90UM2 1 32.02 22.59 1.42 56.78 18.81UM3 1 31.44 20.15 1.56 46.17 22.96

Homo neanderthalensis UI1 5 15.61 24.71 0.63 47.20 9.19UI2 5 17.01 25.40 0.67 41.60 10.45UC 4 20.25 24.28 0.83 55.52 11.20UP3 3 22.95 23.49 0.98 52.31 13.57UP4 4 23.13 22.28 1.04 48.09 15.03UM1 9 24.36 22.97 1.06 48.08 15.29UM2 6 26.05 22.27 1.17 47.72 17.06UM3 5 26.16 21.33 1.22 46.30 18.07LI1 3 10.88 20.63 0.53 33.35 9.14LI2 3 12.51 21.69 0.58 36.59 9.54LC 2 16.13 22.50 0.71 45.37 10.57LP3 2 17.61 19.68 0.89 38.87 14.38LP4 2 20.59 20.69 1.00 39.05 16.06LM1 13 21.59 21.58 1.00 42.96 15.45LM2 6 21.12 20.53 1.03 44.55 15.48LM3 6 19.24 18.93 1.01 37.01 16.78

Fossil Homo sapiens UI1 2 16.74 23.60 0.71 44.50 10.57UI2 2 15.74 22.91 0.69 35.98 11.52UC 2 18.83 21.67 0.87 46.89 12.71UP3 1 26.98 21.46 1.26 45.01 18.74UP4 1 26.81 20.42 1.31 42.61 20.11UM1 4 28.77 22.36 1.28 49.77 18.15UM2 1 25.97 19.82 1.31 43.63 19.83LI1 2 10.25 19.55 0.53 29.45 9.65LI2 3 10.75 19.95 0.53 30.13 9.77LC 4 18.73 23.81 0.77 52.32 10.65LP3 3 21.32 20.46 1.04 42.68 15.81LP4 2 24.15 22.31 1.08 44.18 16.17LM1 6 26.09 21.97 1.19 43.92 18.02LM2 4 27.90 21.80 1.28 49.16 18.31LM3 2 25.61 19.92 1.28 38.82 20.53

Recent Homo sapiens UI1 32 13.46 21.55 0.62 32.73 10.91UI2 31 12.16 19.04 0.64 26.78 12.51UC 22 19.02 20.96 0.91 40.28 14.43UP3 19 22.12 19.99 1.10 39.18 17.69UP4 26 22.90 20.01 1.14 38.01 18.55UM1 40 25.11 20.66 1.22 42.67 18.72UM2 29 28.89 20.61 1.40 43.69 21.40UM3 52 27.13 19.70 1.38 40.96 21.76LI1 16 10.05 18.21 0.55 23.97 11.23LI2 12 11.40 19.23 0.59 27.49 11.28LC 20 16.84 20.89 0.81 40.12 12.91

T.M. Smith et al. / Journal of Human Evolution 62 (2012) 395e411408

Appendix B

Mean values of the components of enamel thickness indices in Homo.

Sample Tooth N c e AET b RET

East African early Homo UC 1 22.06 30.49 0.72 90.98 7.59UP3 1 35.71 26.67 1.34 78.50 15.11UP4 1 36.66 26.18 1.40 76.92 15.97UM1 1 29.70 24.77 1.20 58.82 15.63UM2 1 44.78 26.56 1.69 81.51 18.67

LP3 17 18.08 17.85 1.01 33.16 17.78LP4 17 21.79 18.12 1.20 32.88 21.19LM1 58 21.95 20.37 1.08 40.51 17.02LM2 47 22.15 18.54 1.20 34.44 20.54LM3 45 22.86 18.32 1.25 33.37 21.72

U: maxillary tooth, L: mandibular tooth. See text for description of c, e, AET, b, andRET.

T.M. Smith et al. / Journal of Human Evolution 62 (2012) 395e411 409

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