Allometry, Merism, and Tooth Shape of the Lower Second Deciduous Molar and First Permanent Molar

Allometry, Merism, and Tooth Shape of the LowerSecond Deciduous Molar and First Permanent Molar

Shara E. Bailey,1,2* Stefano Benazzi,2,3 Laura Buti,3 and J.-J. Hublin2

1Department of Anthropology, Center for the Study of Human Origins, New York University, New York, NY 100032Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig D-04103, Germany3Department of Cultural Heritage, University of Bologna, Ravenna 48121, Italy

KEY WORDS allometry; metameric variation; H. neanderthalensis; Homo sapiens; geo-metric morphometrics; outline shape

ABSTRACT

Objectives: This study investigates the effect of allometry on the shape of lower dm2 (dm2) and lower M1 (M1)crown outlines and examines whether the trajectory and magnitude of allometric scaling are shared between Nean-dertals and Homo sapiens.

Methods: Our sample included 164 specimens: 57 recent H. sapiens, 44 Upper Paleolithic H. sapiens, 17 early H.sapiens, and 46 Neandertals. Of these, 59 represent dm2/M1 pairs from the same individuals. Occlusal photographswere used to obtain crown shapes of dm2s and M1s. Principal components analysis (PCA) of the matrix of shapecoordinates was used to explore the pattern of morphological variation across the dm2 and M1 samples. Allometrywas investigated by means of the Pearson product-moment correlation coefficient. Two-block partial least squares(2B-PLS) analysis was used to explore patterns of covariation between dm2 and M 1 crown outlines of matched indi-vidual pairs.

Results: The PCA confirmed significant differences between Neandertal and H. sapiens dm2 and M1 shapes.Allometry accounted for a small but statistically significant proportion of the total morphological variance. The mag-nitude of the allometric contribution to crown shape was stronger among Neandertals than among H. sapiens. How-ever, we could not reject the null hypothesis that the two species share the same allometric trajectory. The 2B-PLSanalysis of the pooled sample of paired individuals revealed a significant correlation in crown shape between dm2and M1. While Procrustes distances differed significantly between dm2 and M1 in Neandertals, it did not among H.sapiens groups.

Conclusions: Our results confirm several of the results obtained by a similar study of upper dm2/M1 (dm2/M1),but there are differences as well. Neandertal dm2/M1 shapes are less derived than those of the dm2/M1. Such differ-ences may support previous studies, which have suggested that different developmental and/or epigenetic factorsaffect the upper and lower dentitions. Am J Phys Anthropol 159:93–105, 2016. VC 2015 Wiley Periodicals, Inc.

Teeth have long been recognized for their durability inthe fossil and archaeological records. Human teeth pro-vide a wealth of information on diet, health, and socialstatus as well as biological and evolutionary relation-ships. Traditionally, greater consideration has beengiven to the morphology of the permanent teeth com-pared with that of the deciduous teeth, and this is forgood reasons: a smaller proportion of deciduous teethare likely to be discovered because there are fewer ofthem (20 vs. 32 in a complete dentition); they have thin-ner enamel and roots, which are more easily damaged;and, in preindustrial humans they are also often quiteworn by the time they are shed.

Despite sometimes being passed over in favor of thepermanent dentition there has been a resurgence ofinterest in the deciduous dentition, especially in the con-text of the human fossil record, (e.g. Zanolli et al., 2010;Benazzi et al., 2011c, 2012, 2015; Bailey et al., 2014a,b;Martin�on-Torres et al., 2014; Harvati et al., 2015). Manyof these studies reflect recent technological advances(e.g. mCT and geometric morphometrics) that have pro-vided new ways to assess dental morphology. Thesestudies, as well as those of recent humans (see below),recognize that because deciduous teeth form quickly andin utero (at birth all deciduous teeth are crown complete:Liversidge and Molleson, 2004) their size and morphol-

ogy at the time of eruption are likely influenced less byenvironment. It is presumed, therefore, that the pheno-type of the deciduous dentition may provide a moreaccurate reflection of an individual’s underlying geno-type than does the phenotype of the permanentdentition.

When preserved, nonmetric traits of deciduous teethhave proven to be highly informative for understandingbiological relationships among living and bioarchaeologi-cally derived human populations (e.g., Sciulli 1977,1998, 2001; Sawyer et al., 1982; Lukacs and Walimbe,1984; Guatelli-Steinberg et al., 2006; Lukacs and Kus-wandari, 2013). They have also been found to be highlyinformative in the context of the human fossil record(e.g., Seny€urek, 1959; Brabant, 1967; Howell and

*Correspondence to: Shara E. Bailey, Department of Anthropology,Center for the Study of Human Origins, New York University, 25Waverly Place, New York, NY 10003, USA. E-mail: [email protected]

Received 4 June 2015; revised 3 August 2015; accepted 11 August2015

DOI: 10.1002/ajpa.22842Published online 2 September 2015 in Wiley Online Library

(wileyonlinelibrary.com).

� 2015 WILEY PERIODICALS, INC.

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 159:93–105 (2016)

Coppens, 1973; Smith, 1978; Korenhof, 1982; Grine,1984; Mallegni and Ronchitelli, 1989; Zanolli and Mac-chiarelli, 2010; Benazzi et al., 2011c, 2012, 2015; Baileyet al., 2014a; Harvati et al., 2015). Unfortunately, exceptin the youngest children, deciduous teeth of fossil homi-nins are often worn, and even after moderate wear,many diagnostic nonmetric dental traits cannot beassessed.

The problem of tooth wear can be circumvented if theenamel-dentine junction is available for study (e.g., Skin-ner et al., 2008’ Bailey et al., 2011) but this is a time-consuming and expensive process. The examination ofcrown outlines also provides a way to side-step the issueof occlusal wear, except in the most extreme cases. Buteven then, if three-dimensional (3D) models are available,cervical outlines can provide taxonomically informativeinformation (Benazzi et al., 2012). For example, cervicaland crown outline shapes of the dm1 and dm2 have beenshown to strongly discriminate between Homo neander-thalensis (hereafter, Neandertals) and H. sapiens (Sou-day, 2008; Benazzi, 2012; Bailey et al., 2014b). Moreover,the shape of the dm2 of H. sapiens and Neandertals arelikely both derived relative to the ancestral condition butin different ways, with H. erectus exhibiting a more inter-mediate and likely ancestral form (Bailey et al., 2014b).

Taxonomically important differences between the dm2sof Neandertals and H. sapiens have also been reported.Tattersall and Schwartz (1999) commented that Nean-dertal dm2s possess a rounder outline than do those ofH. sapiens. These differences were quantified by Souday(2008), Souday and Bailey (2011), and Benazzi et al.(2012). These studies found that Neandertals and H.sapiens could be discriminated quite well based on thedm2 crown and cervical outlines. Souday and Bailey(2011) also noted that the buccal groove of Neandertaldm2s was shifted distally relative to H. sapiens.

Both in the upper and lower dentition, dm2 and M1are quite similar in shape and form. Recent studies havequantitatively supported the close morphological similar-ities between the two teeth both within and across homi-nin species. The same aspects of the M1 that distinguishNeandertals and H. sapiens (namely enlarged, protrud-ing hypocone and metacone reduction) are found also inthe dm2 (Benazzi et al., 2011b; Bailey et al., 2014b).Likewise, the same features that differentiate Neander-tals and H. sapiens M1 crown outlines (buccolingual dis-tal expansion vs. reduction, and convex vs. straightlingual outline shape (Benazzi et al., 2011a) are foundalso in the in the crown and cervical outlines of dm2s(Benazzi et al., 2011c). Although the exact mechanismsthat account for tooth variation along the tooth row arestill unclear, their similarity may be attributed, at leastin part, to the fact that the teeth are derived from thesame dental lamina. Butler’s field theory (Butler, 1939)included the deciduous molars in the “molar field,” and

in this context the dm2 and M1 are best thought of asmeristic elements—serially repeated, yet modified (Bate-son, 1894). The close morphological similarity of dm2and M1 is expected if meristic dental elements representsequential phases of development of the same basic tooth(Dahlberg, 1945; Butler, 1956, 1967a,b, 1971; Kraus andJordan, 1965; Sofaer et al., 1972; Saunders and Mayhall,1982; Smith et al., 1987; Smith, 1989).

Bailey et al. (2014a) investigated the role of size in theunique shape of Neandertal upper molars, and found asmall but statistically significant allometric effect on theshape of dm2 and M1 both between species and withinspecies. Interestingly, the magnitude of the effect wassignificantly stronger in Neandertals than in H. sapiens.In Neandertals as dm2s get larger they take on a shapethat is more similar to M1, and the largest M1s possessthe most skewed outlines. On the other hand, large M1sof H. sapiens do not converge on the shape of similarsized Neandertal M1s. Therefore, Bailey et al. (2014a)concluded that allometry alone could not account for thedifferences observed between these taxa.

Although we might assume that the upper and lowerdentitions are under the same or very similar geneticcontrols this is not necessarily the case. For example,Koh et al. (2010) found fewer genetic correlations of cuspsizes in maxillary compared with mandibular molars.With this in mind, we investigate the effect of allometryon the shapes of dm2 and M1. Since previous work byBenazzi and colleagues (Benazzi et al., 2011a,) has sug-gested that the outlines of dm2 and M1 differentiateNeandertals and H. sapiens in a similar way, wehypothesize that similar allometric effects on tooth sizeshould affect dm2 and M1. We further hypothesize thatthe allometric effects within each taxon should be simi-lar to those observed for the dm2 and M1.

We examined the shapes of dm2 and M1 within individu-als and also made comparisons between H. sapiens andNeandertals. We then investigated the effect of size on theshape of these elements. As was the case for their maxil-lary counterparts, Neandertal dm2 and M1 are larger, onaverage, than those of Upper Paleolithic and recent H.sapiens (see Table 1). Therefore, it is possible that theshape of the M1 and dm2 may be simply a predictable con-sequence of their larger size. We explored this possibilityby assessing static allometry within taxa and evolutionaryallometry between taxa. Along the same lines, one of themost obvious differences between dm2 and M1 is size: in agiven individual the dm2 is on average 25% smaller thanM1 (see Table 1). Therefore, we also examined the meta-meric variation between dm2 and M1 to determine whetheror not shape follows a predictable trajectory based on size.We sought to answer the following questions:

� Do dm2 and M1 crown shapes scale allometrically inH. sapiens and Neandertals?

TABLE 1. Measured crown areas (mm2) of lower dm2 and M1 in matched individual (Bailey, unpublished data)

Early H. sapiens(n 5 2)

Upper PaleolithicH. sapiens (n 5 8)

Recent H. sapiens(n 5 46)

H. neanderthalensis(n 5 3)

dm2 96.05 73.6 75.6 81.95M1 136.4 92.2 99.0 110.3dm2 as a % of M1 0.70 0.80 0.77 0.74

Measurements taken from occlusal crown photographs (see Methods). The early H. sapiens sample comprises anatomically modernH. sapiens individuals predating the Upper Paleolithic. It includes one Aterian individual (Irhoud 3) and one Levantine individual(Qafzeh 15). Note that Aterian individuals possess molars that are substantially larger than those of Levantine early H. sapiens.

94 BAILEY ET AL.

American Journal of Physical Anthropology

� If so, what portion of the shape differences can beaccounted for by allometric scaling?� Does the scaling of the dm 2 and M1 share a common

trajectory and magnitude between Neandertals and H.sapiens?� Do lower and upper dm2/M1 pairs follow similar

patterns?

MATERIALS

Our sample included 164 specimens: 57 recent H.sapiens (RHS), 44 Upper Paleolithic H. sapiens (UPHS),17 early H. sapiens (EHS), and 46 Neandertals (seeTable 2 for details). Teeth were included in the study ifthey were undamaged and unworn-to-moderately worn[Molnar’s stages 1–5 (1971)]. As it is difficult to deter-mine the sex of fossil specimens (especially those repre-sented only by the dentition), we did not consider sex asa variable in this study.

We arbitrarily chose teeth from the left side to repre-sent each individual. However, dentitions and individualteeth of fossil and archaeologically derived specimens,such as those included here, are often incomplete and/ordamaged. In these cases whichever tooth was present orbest preserved was used. Those representing the rightside were mirror imaged in Adobe PhotoshopVR . Studieshave found that when dental asymmetry occurs it doesso randomly with regard to side—a phenomenon calledfluctuating asymmetry. Fluctuating asymmetry is gener-ally considered to be a reflection of an individual’s inabil-ity to buffer against developmental disturbances (VanValen, 1962). Although differences between the shape of

TABLE 2. Sample compositions

ldm2 LM1

Recent H. sapiens (46 matched pairs) 57 46Western Europe 26 24India 4 3South America 7 6Africa (Southern, Eastern, Northern) 20 13

Upper Paleolithic H. sapiens (eight matched pairs) 17 27Lagar Velho X XL’Estelas X XLa Madeleine X XMiesslingtal X XSt. Germain B3 X XSt. Germain B4 X XSt. Germaine B5 X XSunghir 3 X XBruniquel II XFiguier XFontechevade XIsturitz III 1937-119-1950-6 XIsturitz III 1950-5-1 XIsturitz III 1950-7 XKostenki 12 XKostenki 15 XSolutre XAbeille 2 XAbri Pataud XFarincourt XFish Hoek XLa Chaise XLa Chaud 3 XLa Chaud 5 XLa Chaud 80 XLaugerie Basse XLes Rois 3 XLes Rois 14 XLes Rois 16 XLes Rois 1955-5 XLes Rois 1955-148 XLes Rois R50 40 XLes Rois A XPestera cu Oase 1 XVachons 1 X

Early H. sapiens (two matched pairs) 4 13Irhoud 3a X XQafzeh 15 X XEquus Cave H8 XSkhul 1 XDar es-Soltan H4 XDar es-Soltan H5 XDie Kelders 6242 XDie Kelders 6277 XEl Harhoura XKlaises River Mouth XQafzeh 9 XQafzeh 10 XQafzeh 11 XTemara 3a XTemara mandible X

H. neanderthalensis (three matched pairs) 18 28Combe Grenal Ia X XKrapina 53 (Mandible C)a,b X XRoc de Marsala X XArchi XArcy sur cure 29 XBarakai XCova Negra XKebara 1 XKrapina 51 (Mandible B)b XKrapina D62b XKrapina D63b XKrapina D64b X

TABLE 2. Continued

ldm2 LM1

Krapina D65b XKrapina D66b XKrapina D68b XLa Ferrassie 8a XMolare XPech-de-l’Az�e XBreuil H3 XCombe Grenal IV XFossellone 3 XGibraltar II XHortus II XHortus IV XKebara 4a XKrapina 55a,b XKrapina Mandible Da,b XKrapina D80a,b XKrapina D81a,b XKrapina D105a,b XLe Moustier XMalarnaud XMontmaurin XPetit-Puymoyen XPetit-Puymoyen XRegourdou XSt. C�esaire XTabun Series II XTabun Series III XTaddeo XValdegoba VB1-1 XValdegoba VB 1-2 XVindija 11-39 X

a Indicates 2D occlusal crown outline captured from a 3D mCTmodel.b Individuals considered early Neandertals (see text).

ALLOMETRY, MERISM, AND TOOTH SHAPE OF THE DM2 AND M1 95


left and right lower molars has not been quantified, weassume that like tooth size and dental nonmetric traits(see Scott and Turner, 1997 for review) asymmetry israndom, thus the choice of side will not affect the out-come of our results.

METHODS

A Canon EOS Rebel XT digital 8 MP camera equippedwith a macro lens was used to take occlusal images ofthe dm2s and M1s. Only original skeletal and fossilmaterials were used. Images were taken by SEB or CS1

and KP1 under SEB’s supervision. A bubble device wasused to level the camera. Each image included a simi-larly leveled millimeter scale that was placed at approxi-mately the same height as the cusp tips. Individualteeth were oriented so that the cervical border was per-pendicular to the camera’s optical axis. Interobservererror due to differences in image orientation and cameraequipment has been shown to be low and not signifi-cantly greater than intra-observer error (Bailey et al.,2004).

In some cases occlusal images were acquired from vir-tual 3D models based on mCT scans of original speci-mens performed by the Department of Human Evolutionof the Max Planck Institute for Evolutionary Anthropol-ogy. In those cases either an industrial mCT systemand/or desktop system was used and the subsequentvoxel resolutions ranged from 14 to 70 lm. The imagestacks of each tooth were filtered (using a computer pro-grammed macro that employs a three-dimensionalmedian and mean-of-least-variance filter) to improve tis-sue grayscale homogeneity. They were then segmentedinto enamel and dentine components manually withAvizoVR (v6.0). The crown surface was extracted as a 3Ddigital surface model (.ply format). The models of themCT scans were opened in AvizoVR . As was the case forskeletal/fossil material, each tooth was oriented so thatthe cervical border was perpendicular to the optical axisin both mesio-distal and bucco-lingual directions(Benazzi et al., 2009). AvisoVR software was used to addan appropriate scale and a screen shot of the occlusalsurface (analogous to taking a digital photograph) was

taken and saved as a .jpg file. A recent study has shownthat there is no significant difference between crownoutlines obtained from photos and virtual 3D models(Buti, 2013).

Screen shots and digital images were imported intoAdobe PhotoshopVR . The (now 2D) images were then rotatedso that each tooth approximated anatomical position. Back-grounds were removed and image contrast was adjusted toprovide a clear distinction between the crown outline andthe background. Finally, each image was scaled to approxi-mately the same size and resolution (300 dpi).

Even in moderately worn teeth, interproximal wearmay distort the mesial and/or distal aspects of the crownoutline. Where this was the case, the outline was recon-structed by estimating the original mesial and/or distalborders (see Wood and Abbott, 1983; Wood and Engleman,1988; Bailey, 2004; G�omez-Robles et al., 2007). These esti-mations were based on the buccolingual extent of thewear facet and the overall contour of the tooth (see Fig. 1)and all estimations were made by one person (SEB).

To analyze crown outlines occlusal images of the M1sand dm2s were imported in Rhino 4.0 Beta CAD environ-ment (Robert McNeel & Associates, Seattle, WA) andaligned to the xy-plane of the Cartesian coordinate sys-tem. The crown outline was manually digitized for eachtooth using the spline function, and oriented with thelingual side parallel to the x-axis (for more details aboutthe orientation protocol see Benazzi et al., 2012).

Outlines were first centered superimposing the cent-roids of their area and then represented by 24 pseudo-landmarks obtained by equiangularly spaced radialvectors emanating from the centroid (Benazzi et al.,2011a). The first radius is directed buccally and parallelto the y-axis of the Cartesian coordinate system (Fig. 2).Size information from the centered and oriented outlineswas removed with a uniform scaling of the pseudoland-mark configurations to unit centroid size (Benazzi et al.,2011b,c,2012). As emphasized by Benazzi et al. (2012),this procedure differs from the commonly used general-ized Procrustes analysis (GPA) because rotation andtranslation are constrained by anatomical considerations.After being scaled to unit centroid size, the shape coordi-nates can be considered Procrustes shape coordinates.

Permutation tests (n 5 1,000) of Procrustes distances(q 5 the square root of the sum of squared differences

Fig. 1. Heavily worn lower M1 illustrating editing process. The tooth is flipped to represent the left side and corrected forwear.

1See Acknowledgements

96 BAILEY ET AL.


between the positions of corresponding pseudoland-marks) between mean shapes were carried out to testthe statistical significance of molar (dm2 and M1) shapedifference within and between Neandertals and H. sapi-ens (which includes EHS, UPHS, and RHS), andbetween tooth classes. For each permutation test, speci-mens were randomly reassigned with respect to group,either tooth class or species, and the Procrustes distancebetween the new group means was then computed(Good, 2000; Zelditch et al., 2004).

A principal components analysis (PCA) of the matrix ofshape coordinates was carried out to explore the patternof morphological variation across the dm2 and M1 sam-ples. Shape variation related to size (allometry) was firstinvestigated by Pearson product-moment correlation coef-ficient (r) of shape variables (PCs) on the logarithm ofcrown base area. To measure crown base areas, (i.e., toothsize) images were imported into SigmaScanVR Pro, cali-brated using the scale in each photograph and then meas-ured using the trace function. The null hypothesis ofshared allometric trajectory of the groups was assessedby measuring the angle between allometric vectors, calcu-lated as the dot product of regression coefficients (Cardiniand Elton, 2007), while differences in vector magnitude(length) were computed as the absolute difference in vec-tor lengths. The statistical significance of observed vectorangle and magnitude was determined using a permuta-tion test (n 5 1,000), where the two groups were com-bined and molars (dm2s and M1s) were randomlyreassigned to species before computing the angular differ-ences (Good, 2000; Zelditch et al., 2004).

Finally, two-block partial least squares (2B-PLS) anal-ysis [also called singular warp analysis when applied toProcrustes coordinates (Rohlf and Corti, 2000; Booksteinet al., 2003)] was used to explore patterns of covariationbetween dm2 and M1 crown outlines in a subsamplecomposed of the 59 individuals with dm2/M1 pairs. Themajority (46) of these matched pairs were from RHS.For the fossil individuals, 8 Upper Paleolithic H. sapi-ens, 2 early H. sapiens, and 3 H. neanderthalensis werematched pairs. So as to compare only the patterns ofcovariation, irrespective of group mean differences andallometric differences (Mitteroecker and Bookstein,2008; Mitteroecker et al., 2012), we first centered eachtaxon removing the within-group mean (independentlyfor dm2s and M1s), and then regressed out size (loga-rithm of crown base area) from the shape coordinates in

order to remove allometric shape variation. The non-centered shape coordinates were then projected on thecomputed PLS vectors to produce the singular warp(SW) scores, which reflect mean differences if, in fact,such differences exist. A permutation test was used toassess the statistical significance of the Pearson product-moment correlation coefficient (r) between the first pairof singular warps (SW1s). The data was processed andanalyzed through software routines written in R (RDevelopment Core Team, 2012).

RESULTS

Shapes of the dm2 and M1

Neandertal M1s are significantly different with regardto within-tooth class Procrustes distances of crown shape(Table 4), from those of RHS and UPHS (P < 0.001), butnot from those of EHS (P 5 0.099). RHS and UPHS M1sdo not differ significantly from one another, but both dif-fer significantly from EHS (P < 0.04). A principal compo-nents analysis of tooth shapes shows that NeandertalM1s generally receive negative scores for PC1 and conse-quently occupy the left side of Figure 3, but they are dis-tributed randomly along PC2. The distribution of H.sapiens individuals overlaps completely that of Neander-tals. With generally positive scores for PC2, early H.sapiens M1s are found primarily in the upper half of Fig-ure 3. By contrast, Upper Paleolithic and recent H. sapi-ens specimens, do not show any patterning for eitherPC1 or PC2.

Neandertals possess dm2s that differ significantlyfrom UPHS and RHS (P<0.001), but not EHS (Table 4),while the H. sapiens subgroups do not differ significantlyfrom one other (RHS–UPHS: q 5 0.0089, P 5 0.067;RHS–EHS: q 5 0.0111, P 5 0.491; UPHS–EHS: q 5

0.0131, P 5 0.444). Figure 4 shows the results of a prin-cipal components analysis of dm2 shapes. The distribu-tion of individuals along PC1 is generally random,although Neandertals show a narrower range of varia-tion in dm2 shape than do either UPHS or RHS (RHSbeing the most variable). In fact, nearly all Neandertaldm2s possess negative scores and fall in the lower half ofFigure 4. In contrast, UPHS dm2s more often possesspositive scores for PC2 and are thus more heavily dis-tributed on the top half of Figure 4. As is seen for PC1,the distribution of PC2 scores for dm2s of RHS appearsrandom. As a result, convex hulls drawn around the

Fig. 2. Illustration of landmark acquisition and orientation.



Fig. 3. PCA plot of M1 shapes.

Fig. 4. PCA plot of dm2 shapes.

98 BAILEY ET AL.


distribution of scores for the dm2s of UPHS and Nean-dertals show moderately strong separation (as reflectedin significant shape differences), whereas the distribu-tion of component scores for RHS dm2s encompassesnearly all the other specimens.

Relationships between dm2 and M1

Permutation tests (Table 5) show that between toothclasses (dm2 against M1), Procrustes distances are signifi-cantly different in Neandertals (q 5 0.0143, P < 0.001),approach statistical significance in RHS (q 5 0.0069,P 5 0.0569), but are not significantly different in eithergroup of fossil H. sapiens (UPHS: q 5 0.0097, P 5 0.157;EHS: q 5 0.0149, P 5 0.491). These differences can beobserved in Figure 5, where Neandertal dm2s have pre-dominantly negative scores for PC1, while proportionatelymore M1s have positive scores. The shapes associatedwith these differences reflect the fact that the smallerdm2 tends to be more rectangular (i.e., narrower buccolin-gually), whereas the larger M1s tend to be more square/rounded (i.e., broader buccolingually) (Tables 3–5).

The allometric trajectory across the dm2–M1s morpho-space for the two groups (Neandertals and H. sapiens)was computed by multivariate regression of shape varia-bles on crown base area (Fig. 6). When the two groups

are combined, this analysis reveals a small but signifi-cant allometric effect that accounts for 6.8% of the totalvariance in dm2 and M1 crown shape. However, whenthe two taxa are considered separately, the allometriceffect explains a larger fraction of variance in Neander-tals (20.7%) than in H. sapiens (14.5%). Although theallometric trajectories are not parallel, angular differen-ces between Neandertal and H. sapiens dm2/M1 allomet-ric vectors do not reach statistical significance (308, P 5

0.07). Also, the magnitude of the interspecies allometricvariation does not differ significantly between the twogroups (P 5 0.113). Results do not change when the firstthree principal component vectors are considered formultivariate regression analysis, either for angle (24.58,

Fig. 5. Combined PCA plot of dm2 and M1 shapes.

TABLE 3. Within-tooth class Procrustes distances (M1)

N-M1 EHS-M1 UPHS-M1

EHS-M1 0.0113UPHS-M1 0.0144a 0.0146a

RHS-M1 0.0147a 0.0145a 0.0071

a Significant difference at P<0.05.Abbreviations are the same as provided in Table 3.

TABLE 4. Within-tooth class Procrustes distances (dm2)

N-dm2 EHS-dm2 UPHS-dm2

EHS-dm2 0.0139UPHS-dm2 0.0186a 0.0131RHS-dm2 0.0182a 0.0111 0.0089

Abbreviations are the same as provided in Table 3.a Significant difference at P<0.05.

TABLE 5. Between-tooth class Procrustes distances

N-M1 EHS-M1 UPHS-M1 RHS-M1

N-dm2 0.0143a

EHS-dm2 0.0149UPHS-dm2 0.0097RHS-dm2 0.0069

a Significant difference at P<0.05.N, Neandertals; EHS, early H. sapiens; UPHS, Upper Paleo-lithic H. sapiens; RHS, recent H. sapiens.



P 5 0.08) or magnitude (P 5 0.077). Such results sug-gest that we cannot reject the null hypothesis of similarallometric trajectory from dm2s to M1s for Neandertalsand H. sapiens.

Considered separately (Fig. 7), within-species allomet-ric trajectories of dm2s and M1s were not significantlydifferent for either Neandertals (62.78, P 5 0.848) or H.sapiens (98.88, P 5 0.818). Similar lack of significant

Fig. 6. Between species allometric trajectories for dm2-M1 shapes. Black line represents H. sapiens red line representsNeandertals.

Fig. 7. Within species allometric trajectories for dm2 and M1 shapes.

100 BAILEY ET AL.


differences between Neandertals and H. sapiens wereobserved for within-tooth class allometric trajectories forM1s (56.48, P 5 0.734) and dm2s (67.38, P 50.766).

The first pair of SWs based on the 2B-PLS analysis ofthe 58 individuals represented by dm2/M1 pairs explainsabout 35% of the covariance between dm2 and M1 crownoutline shape coordinates (Fig. 8). The analysis reveals acorrelation (r) of 0.51 between dm2 and M1 crown shapein our sample (admittedly dominated by RHS individu-als), a value that approaches statistical significance (P 5

0.056). This result emphasizes that when a M1 crownshows marked mesiodistal expansion (positive SW M1 inFig. 8), or enlargement of the protoconid resulting in agenerally sub-square shape outline (negative SW1 M1 inFig. 8), the same trend can be observed in the dm2

crown. Nonetheless, the PLS plot shows also that dm2

crowns are generally more expanded mesiodistally thanthose of M1s.

DISCUSSION

Comparisons for results of crown shapes

The results of this study support earlier findings,which show that the shapes of dm2 and M1 differ signifi-cantly between Neandertals and H. sapiens. Here, asbefore (Benazzi et al., 2011a, 2012), we found Neandertaldm2s and M1s are marked by an expansion of the disto-buccal outline and by a convex lingual outline, while H.sapiens dm2s and M1s are associated with a reduction ofthe distobuccal outline and a lingual outline that is lessconvex. The fact that M1s possess a less rectangularshape than the smaller dm2s is consistent with the

results from Singleton et al. (2011) who found thatamong individuals of the genus Pan larger molars havesquarer crowns.

A comparison of PCA plots of tooth shapes obtainedhere differ somewhat from those of earlier studies inwhich better graphical separation of the groups wasfound (Benazzi et al., 2011a, 2012). These differences arelikely the consequence of different sample compositions.In the earlier studies the Neandertal and UPHS sampleswere less than half the size as in the present study. Inaddition, the sample compositions overlap in only a fewspecimens: Benazzi et al.’s (2012) UPHS sample sharesonly one specimen with the current study and in theearlier study the Neandertal sample includes a higherproportion of early Neandertals (see Table 2) than wereincluded here. Finally, in the present study we includeda substantially larger number of RHS representing awider geographic area (Africa, Asia, South America,Europe) than that of the studies by Benazzi et al.(2011a, 2012). Even with the greater degree of overlapthat comes with larger sample sizes, for both dm2 andM1 the Neandertal group forms a well-defined cluster,which supports their dental morphological separationfrom H. sapiens (especially UPHS) found in earlierstudies.

Bailey (2002b) previously failed to find significant dif-ferences among fossil groups for her measures of M1

crown shape, which included relative cusp areas andcusp angles of the occlusal polygon. Although differencesin relative cusp areas are at least partially reflected indifferences in crown outline shape (Gomez-Robles et al.,2007, 2012; Bailey et al., 2014a), it appears that relative

Fig. 8. PLS Plot of matched lower dm2/M1 pairs.



cusp area and occlusal polygon angles do not fully cap-ture the shape differences between the two groups inthe M1. Smaller sample sizes in Bailey’s (2002b) studymay have also played a role in the lack of significant dif-ferences found among groups. In sum, while significantdifferences in crown outline shape of the M1s existbetween Neandertals and H. sapiens, there is a greaterdegree of overlap in shape than has been previouslyreported. As such, nonmetric traits of the M1s (e.g., trig-onid crests: Bailey 2002a; Bailey et al., 2011; Mart�ınezde Pinillos et al., 2014) may be more reliable than crownoutlines in discriminating these two groups.

It is generally accepted that the deciduous secondmolar is more conservative evolutionarily than the per-manent first molar based on its higher frequency of pre-sumed “primitive” traits (e.g., Dryopithecus Y-5 molarpattern) (Butler, 1956, 1971; Saunders and Mayhall,1982). In a previous morphometric study of dm2/M1 pairsin recent and fossil hominins Smith et al. (1997) con-cluded that the dm2 of recent H. sapiens retains theprimitive condition based on its greater similarity to thedm2 and M1 of early H. sapiens. The results of the pres-ent study are in agreement with this general conclusion.That is, Neandertal and H. sapiens (RHS and UPHS)dm2s appear to maintain a more conservative morphol-ogy (i.e., more similar to EHS), while the M1 appears tobe more derived in RHS and UPHS (indeed in Table 4,EHS M1s are significantly different from UPHS andRHS M1s).

Comparison to upper dm2/M1 pairs

The results of this study on the dm2 and M1 crownshapes are similar to a previous study on dm2 and M1 ina number of ways (see Bailey et al., 2014a). First, inboth cases dm2 and M1 crown shapes differ significantlyin Neandertals but not among the various groups of H.sapiens considered. Second, in both cases moderate-to-strong correlations are found between dm2 and M1(r 5 0.62 for dm2/M1 pairs and .51 for dm2/M1 pairs).Third, in both cases Neandertals and H. sapiens (withthe exception of EHS for the lower molars) possess dm2sand M1s that differ significantly in shape, with the dm2appearing less derived than the M1. Finally, in bothcases the allometric trajectories found for dm2s and M1sdid not differ significantly from one another and theallometric trajectories of neither dm2/M1 nor dm2/M1

pairs differed significantly between Neandertals and H.sapiens.

We also found some differences between the two stud-ies. First, there is a greater overlap between H. sapiensand Neandertals in dm2 and M1 shapes compared withtheir maxillary counterparts. In the present study Nean-dertal dm2/M1 shapes do not differ significantly fromthose of EHS, whereas the previous study by (Baileyet al., 2014a) found that the shapes of the dm2 and M1

do. Moreover, dm2/M1 crown shapes of RHS and UPHSdiffered significantly from that of EHS, whereas in theprevious study of dm2/M1 crown shapes none of the H.sapiens groups differed significantly from each other.Second, the correlation between the shapes of the dm2and M1 was weaker in the lower vs. upper molars (0.51vs. 0.62, respectively). The correlation between dm2/M1

shapes was highly significant (P < 0.001) in the previousstudy but only just approached statistical significancefor the dm2/M1 pairs in this study (P 5 0.056). The pro-portion of variance in dm2/M1 shapes in the lower

molars due to allometry is less than half that of theupper molars (6.8% vs. 16.2%, respectively). Moreover,although in both studies allometry accounts for a largerproportion of shape differences in molars among Nean-dertals than among H. sapiens (20.7% vs. 14.7%, respec-tively for the dm2/M1), the differences betweenNeandertals and H. sapiens is nearly seven timesgreater in the upper dentition (70.2% vs. 11.5%).

The points of divergence between the studies of thelower and upper dm2/M1 pairs are of interest. Thegreater degree of overlap in molar shape between Nean-dertals and H. sapiens in the lower versus upper molarssuggests that lower molar shape may be more conserved(i.e., more similar to EHS) than is the case for the uppermolars (see Tables 4 and 5). The lower molars may alsobe marked by a greater degree of integration. Gomez-Robles and Polly (2012) have suggested that, at leastwith regard to relative tooth size, the more stable envi-ronment of the mandible may result in the lower denti-tion of hominins being more highly integrated, whereasthe upper dentition may be more weakly integrated andthus more likely to respond to changes in the craniumand in the face. Exactly how changes in the face andcranium affect molar shape is unknown.

Since it is presumed that serial homologues such asdm2/M1 are governed by the same genes we wouldexpect them to be morphologically similar (see Weiss,1994). Bolk (1916) noted the greater similarity betweendm2 and M1 than between M1 and M2/M3. Differencesbetween dm2 and M1 are expected due to slight varia-tion in developmental processes and/or stronger environ-mental influences on the later forming tooth (M1). Wemight expect environmental influences to have similareffect on upper and lower dentitions. Moorrees and Reed(1964) found similar correlation coefficients betweenmesiodistal lengths of dm2 and M1 in lower and upperdentitions (0.53 and 0.51, respectively). On the otherhand, we found that dm2/M1 pairs were more stronglycorrelated than dm2/M1 pairs. An earlier study byBenazzi et al. (2011a) also found that the associationbetween shape and size is different in upper and lowerM1s.

Previous studies have suggested that there is a com-plex relationship between the teeth of the upper andlower jaws. On the one hand some degree of integrationis to be expected in order to maintain proper occlusion(Marshall and Butler, 1966; Butler, 1991; Van Valen,1994). Yet, on the other hand, the developmental andevolutionary constraints acting upon the maxillary andmandibular dental elements are not identical. Studies ofbaboon dental metric and nonmetric traits have sug-gested that similarities between the maxillary and man-dibular dental elements are due to similar overlappingbut nonidentical sets of genes (Rizk et al., 2008). Thus,although there should be integration within each jaw,we should expect some independence between them.

This study did not examine the correlation betweenthe distobuccal expansion observed in Neandertal dm2

and M1 outlines and the distolingual expansion observedin the dm2 and M1 outlines. There are few fossil individ-uals who preserve both upper and lower molars; how-ever, we have a large sample of recent H. sapiens thatdo. The obvious next step then is to investigate thesecorrelations to further explore the degree of integrationbetween elements of the upper and lower dentitions ofrecent members of the genus Homo.

102 BAILEY ET AL.


CONCLUSIONS

In this study we investigated how merism and allome-try are expressed in mandibular molar shapes. We chosethe dm2 and M1 because of their morphological similar-ity, early development and because of the hypothesizedgreater evolutionary conservation of the dm2 relative tothe M1.

There was a moderate correlation in crown shape ofdm2/M1 pairs that just reached statistical significance.Even so, the shape of the dm2 differed significantly fromthat of the M1 in Neandertals, while this was not thecase for H. sapiens. These shape differences appear to beinfluenced, at least in part, by positive allometry; for inboth taxa larger M1s possess more square outlines whilesmaller dm2s possess narrower oval or rectangular out-lines. Allometry explained a greater proportion of varia-tion among Neandertals than among H. sapiens, butneither the magnitude nor allometric trajectories weresignificantly different between the two taxa.

Perhaps even more interesting were the differencesbetween this study of dm2/M1 pairs and the previouswork on dm2/M1 pairs (Bailey et al., 2014a). Our resultssuggest that different developmental and/or epigeneticfactors affect the upper and lower dentitions. Futurework will investigate differences in integration furtherby examining upper and lower dm1, dm2 and M1 triadswithin individuals.

ACKNOWLDEGMENTS

The authors thank the Associate Editor and anonymousreviewers for their useful comments and suggestions,which have helped improve the manuscript. For access tospecimens the authors thank the following institutions:Museum Fur Vor-und Fruhgeschichte, Berlin (W. Men-ghin), NESPOS Society (R Macchiarelli), Musee d’Art etArcheologie de la ville de Perigueux (V. Merlin-Anglade),Institut Pal�eontologie Humaine, Paris (H. de Lumley, AVialet), Musee de l’Homme, Paris (P. Mennecier), MuseeNational de Prehistoire, Les Eyzies (J.-J. Cleyet-Merle),Musee d’Archeologie Nationale de Saint-Germain-en-Laye(P. P�erin), Laboratoire de Pal�eontologie Humaine et dePr�ehistoire, Marseille (M.-A. de Lumley and F. Marchal);Museum of P�erigord (V. Merlin-Anglade); Mus�eum d’His-toire Naturelle, Montauban (E. Ladier); NaturhistorischesMuseum Wein (M. Nicola), Hrvatski Prirodoslovni Muzej(J. Radovcic), Hrvatska Akademija Znanosti I Umjetnosti(P. Rudan, J. Braikovic), Direction de l’Arch�eologie ServicePublic de Wallonie, Liege (M. Toussaint), Magyar Term�es-zettudom�anyi M�uzeum (Z. Guba), Natural HistoryMuseum, London (C. Stringer, R. Kruszynski), Universityof Cape Town (A. Morris), University of Witwatersrand (N.Pather), Museu Nacional de Arquelogia, Lisbon (A. San-tos), Museo Prehistoria, Valencia (A. Sanchis), Museo deBurgos (M. Negro Cobo), Universit�a di Roma, La Sapienza(R Sardella), Universit�a degli Studi di Siena (A. Ronchi-telli), Universit�a di Turin (G. Giacabini), Universit�a diPisa (F. Mallegni), Instiut National de Sciences du Patri-moine et de l’Arch�eologique, Mus�ee Arch�eologique deRabat (M.A. El Hajraoui, A. Ban-Nicer, S. Raoui), Instituteand Museum of Anthropology, Moscow (A. Buzhilova, V.Kharitonov), Museum of Anthropology and Ethnography,St. Petersburg (V. Moiseyev, Dr. Balueva, E. Veselov-skaya), Oddeleni Paleolitu a Paleoetnologie Doln�ıV�estonice (J. Svoboda), Sackler School of Medicine, TelAviv University (Y Rak), Rockefeller Museum, Jerusalem

(F. Ibrahim), American Museum of Natural History (I. Tat-tersall, G. Garcia), National Museum of Natural History(D. Hunt), Washington University, St. Louis (E. Trinkaus).The authors thank Claudia Astorino for assistance withimage processing, as well as Kathleen Paul and CarolineSouday who gathered images of some of the recent humangroups under the supervision of SEB. For scanning assis-tance the authors thank Heiko Temming and PatrickSchoenfeld. Data collection for this project was funded bythe LSB Leakey foundation and the Max Planck Society.

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Allometry, Merism, and Tooth Shape of the Lower Second Deciduous Molar and First Permanent Molar