AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 00:00–00 (2014)

Allometry, Merism, and Tooth Shape of the Upper Deciduous M2 and Permanent M1 Shara E. Bailey,1,2* Stefano Benazzi,2 and Jean-Jacques Hublin2 1 2

Department of Anthropology, Center for the Study of Human Origins, New York University, New York, NY 10003 Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig D-04103, Germany KEY WORDS allometry; metameric variation; deciduous molar; H. neanderthalensis; Homo sapiens; geometric morphometrics; outline shape

ABSTRACT The aims of this study were to investigate the effect of allometry on the shape of dm2 and M1 crown outlines and to examine whether the trajectory and magnitude of scaling are shared between species. The sample included 160 recent Homo sapiens, 28 Upper Paleolithic H. sapiens, 10 early H. sapiens, and 33 H. neanderthalensis (Neandertal) individuals. Of these, 97 were dm2/M1 pairs from the same individuals. A two-block partial least squares analysis of paired individuals revealed a significant correlation in crown shape between dm2 and M1. A principal component analysis confirmed that Neandertal and H. sapiens dm2 and M1 shapes differ significantly and that this difference is primarily related to hypocone size and projection. Allometry accounted for a small but significant proportion of the total morphological variance. We

found the magnitude of the allometric effect to be significantly stronger in Neandertals than in H. sapiens. Procrustes distances were significantly different between the two tooth classes in Neandertals, but not among H. sapiens groups. Nevertheless, we could not reject the null hypothesis that the two species share the same allometric trajectory. Although size clearly contributes to the unique shape of the Neandertal dm2 and M1, the largest H. sapiens teeth do not exhibit the most Neandertal-like morphology. Hence, additional factors must contribute to the differences in dm2 and M1 crown shape between these two species. We suggest an investigation of the role of timing and rate of development on the shapes of the dm2 and M1 may provide further answers. Am J Phys Anthropol 000:000–000, 2014. VC 2014 Wiley Periodicals, Inc.

Teeth are well-known for their abundance and excellent preservation in the fossil record. For these reasons, they provide important information on taxonomy, as well as biological relationships among human populations in the recent and distant past. Preservation in the fossil record tends to be biased toward postcanine teeth (premolars and, especially, molars). This is because their propensity for multiple roots provides them with a stronger “anchor” in the jaw and they are better retained postdeposition. This bias is perhaps even more pronounced for the deciduous dentition, for once deposited small and fragile deciduous incisors and canines have little chance of surviving intact. Not surprisingly then, the number of studies on human molar variation far exceeds the number of studies on anterior tooth variation, with the exception of shovel-shaped incisors (Hrdlicˇka, 1920; Dahlberg and Mikkelsen, 1947; Korenhof, 1960; Carbonell, 1963; Hanihara et al., 1964; Suzuki and Sakai, 1964, 1973; Erdbrink, 1965; Portin and Alvesalo, 1974; Grine, 1981; Wood and Abbott, 1983; Mizoguchi, 1985; Morris, 1986; Beynon and Wood, 1987; Hartman, 1988; Macho and Moggi-Cecchi, 1992; Crummett, 1994; Bailey, 2004b; Skinner et al., 2009; Gomez-Robles et al., 2010; Bailey et al., 2011). Molars possess more complex occlusal surfaces than the other teeth and their morphological variants (cusp 6, middle trigonid crest, metaconule, hypocone, etc.) have proved to be useful in the studies of recent and fossil humans (Harris and Bailit, 1980; Berm udez de Castro and Martınez, 1986; Keene, 1994; Bailey et al., 2011). Both deciduous and permanent molars have been studied, but there is a tendency to focus on the permanent molars, especially the first molar

because of its designation as the “key” tooth in the permanent molar field (Butler, 1939; Dahlberg, 1945). Butler’s field concept (Butler, 1939) recognized three dental morphogenetic fields that act to influence final tooth form: incisor, canine, and molar. Butler believed that premolars represent altered anterior members of a permanent molar field. When applying Butler’s concept to humans, Dahlberg (1945) added a premolar field to the otherwise three-field paradigm of the permanent dentition. Although Dahlberg never specifically indicated how many (or which) tooth fields were represented by the deciduous teeth, in subsequent morphological studies, he included deciduous second molars as members of the “molar” tooth district (Dahlberg, 1950). The relationship between the deciduous and the permanent molars is unusual compared to that between the anterior teeth. The deciduous incisors and canines are replaced by permanent teeth that are broadly similar in morphology. In contrast, although deciduous molars are

Ó 2014 WILEY PERIODICALS, INC.

Grant sponsors: The LSB Leakey foundation, The Max Planck Society. *Correspondence to: Shara E. Bailey, Shara E. Bailey, Department of Anthropology, Center for the Study of Human Origins, New York University, 25 Waverly Place, New York, NY 10003, USA. E-mail: [email protected] Received 17 October 2013; accepted 14 January 2014 DOI: 10.1002/ajpa.22477 Published online 00 Month 2014 in Wiley Online Library (wileyonlinelibrary.com).

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S.E. BAILEY ET AL. 1

often referred to as premolars, they do not bear a strong resemblance to the permanent premolars that replace them. Instead, the anterior deciduous molar does not resemble any of the permanent teeth closely; and, despite differences in size, the distal deciduous molar resembles, quite remarkably, the permanent first molar. Although we do not know the exact mechanisms that account for tooth variation along the tooth row, the morphological similarity between the deciduous second molar (dm2) and the permanent first molar (M1) can be attributed, at least in part, to the fact that they share a developmental origin in the same dental lamina. As the permanent molars are not replaced, technically they are part of the primary dentition. Therefore, the dm2 and M1 are best thought of as meristic elements (those whose structure is serially repeated within an organism) within the same dental field (Bateson, 1894). Recent studies suggesting that the dm2 should be considered the “key” tooth of the molar field, including the permanent molars, supports this view (Farmer and Townsend, 1993; Bockmann et al., 2010). Meristic dental elements have been interpreted as representing sequential phases of the development of the same basic tooth (Dahlberg, 1945; Butler, 1956, 1967a, b, 1971; Kraus and Jordan, 1965; Sofaer et al., 1972; Saunders and Mayhall, 1982; Smith et al., 1987; Smith, 1989). Under this paradigm, (as well as Edmond’s (1960) Zahnreihen concept) the close similarity observed between the dm2 and the M1 is expected. As the dm2 forms earlier (initiates mineralization at 5 months in utero and is crown complete by 1 year: (Liversidge and Molleson, 2004)) and more rapidly (Massler and Schour, 1946) than the M1, its size and form are often considered to be under stronger genetic control and less influenced by environment (Sofaer et al., 1972). Teeth that develop early are also thought to be more evolutionarily conservative (Sofaer, 1973; Alberch et al., 1979; Alberch, 1980; Smith et al., 1997). If so, the morphology of the dm2 should be more primitive than that of the M1. Studies comparing the crown morphology of dm2 and M1 have generally supported this hypothesis, based on its higher frequency of “primitive” traits such as the Dryopithecus lower molar pattern (Jorgensen, 1955, 1956; Smith et al., 1987; Aguirre et al., 2006) and cusp 7 (Suzuki and Sakai, 1973; Smith et al., 1987) or based on lower morphological (Saunders and Mayhall, 1982) and metrical (Farmer and Townsend, 1993) variability, as well as its greater stability in the timing of eruption (Bockmann et al., 2010). Most comparisons between dm2 and M1 have been based on a cross-section of individuals as opposed to within individuals (Moorrees et al., 1957; Brabant, 1967; Suzuki and Sakai, 1973; Sciulli, 1977, 1979; Grine, 2005). Comparisons between the dm2 and the M1 in the same individual are meaningful from both developmental and evolutionary viewpoints. Saunders and Mayhall (1982) compared dm2 and M1 within individuals and found significant correlations for Carabelli’s trait, cusp 6, cusp 7, and protostylid expression. Their results contrast somewhat with the findings by Edgar and Lease (2007) who found lower correlation between deciduous and permanent molar morphology (deflecting wrinkle and Carabelli’s trait only). Smith et al.’s (1997) morpho1

In particular, by the comparative morphology/paleontological community.

American Journal of Physical Anthropology

metric study found that the lower dm2 and M1 of fossil humans were more similar to each other than were the lower dm2 and M1 of recent humans. They concluded that the deciduous second molar of recent humans retained the primitive state for Homo sapiens. Recently, there has been a renewed interest in the deciduous molars of fossil hominins (Souday, 2008; Bayle et al., 2010; Zanolli et al., 2010; Benazzi et al., 2011c; Bailey et al., 2013). Of particular interest are comparisons between H. neanderthalensis (hereafter Neandertals) and H. sapiens. Neandertals occupy an important position in the study of human evolution as they are the best known and one of the best preserved of our fossil relatives.2 The evolutionary place of Neandertals (e.g., continuity vs. discontinuity with H. sapiens) has long been debated (Br€ auer, 1984; Stringer et al., 1984; Smith, 1992; Stringer, 1992; Wolpoff et al., 1994; Wolpoff, 2001) but most researchers now accept genetic evidence for minimal admixture between the two (Green et al., 2010). Unfortunately, this does not inform us much on the question of the specific status of Neandertals, as even good biological species can, and do, interbreed and occasionally produce viable and fertile offspring (Holliday, 2003). Regardless of their specific status, studies of the dental differences (permanent or deciduous) between Neandertals and H. sapiens are necessary to assign isolated teeth to taxa when the period of interest spans that of both species (Bailey et al., 2009; Benazzi, 2012). They also have the potential for informing us on differences in growth and development between the species. Studies of the permanent dentition have concluded that Neandertals possess a unique combination of highand low-frequency traits (Bailey, 2007). Some teeth (lower fourth premolar, lower molars, upper incisors, and upper first molar) are more diagnostic than others because they possess traits that have been interpreted either individually (M1 small relative occlusal polygon area) or in combination (P4 asymmetry 1 transverse crest 1 multiple lingual cusps) as derived relative to H. sapiens (Bailey, 2002, 2004a, 2007). No such comparative analysis of Neandertal and H. sapiens deciduous dental morphology has been completed but one is currently underway (Bailey, in preparation). Because of its status as the “key” (most evolutionarily stable) tooth in the permanent molar field, the M1 has played an important role in the analysis of hominin dental variation. As noted above, it is also one of the most diagnostic teeth of Neandertals. Some of the unique qualities of Neandertal M1 morphology are also observed in the dm2. For example, like the M1, the Neandertal dm2 tends to have thinner enamel and a greater proportion of dentine compared to H. sapiens (Benazzi et al., 2011b). In addition, the uniquely skewed upper M1 (M1) crown shape (Bailey, 2004b; Gomez-Robles et al., 2007; Benazzi et al., 2011a) is mirrored in upper dm2 (dm2) crown and cervix shape (Souday, 2008; Benazzi et al., 2011b; Bailey et al., 2013). Studies have suggested that both the thin M1 enamel (Olejniczak et al., 2008) and the skewed M1 shape (Bailey, 2004b; Gomez-Robles et al., 2007) are derived, rather than primitive, features of Neandertals. As it is presumed that sequential teeth (in this case dm2 and M1) are governed by the same genes, we would expect strong morphological similarity between them. 2

The Krapina sample, alone, preserves nearly 200 teeth (Wolpoff, M., 1979. The Krapina dental remains. Am. J. Phys. Anthropol. 50, 67-114.)

ALLOMETRY, MERISM AND TOOTH SHAPE OF DM2 AND M1

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2

2

1

TABLE 1. Basic statistics (average, range, and number of individuals) for measured crown area (mm ) of dm and M and relative size of dm2 to M1 in matched individuals Tooth 2

dm M1 dm2/M1

RHS

UPHS

EHS

Neandertals

74.2 (59.7–100.0) n 5 80 97.4 (79.0–124.1) n 5 99 0.76 (0.64–0.92) n 5 87

78.9 (63.1–86.2) n 5 6 101.5 (81.7–123.1) n 5 7 0.80 (0.68–0.92) n 5 6

85.6 (77.9–97.5) n 5 4 126.4 (98.0–146.3) n 5 7 0.83 (0.73–0.89) n 5 3

87.9 (70.8–108.8) n 5 15 114.1 (91.6–153.4) n 5 18 0.81 (0.67–0.93) n 5 7

Note: Differences between RHS, UPHS and Neandertals are significant for both dm2 and M1 (P < 0.01). However, differences between EHS and Neandertals are not significant for either tooth. In all groups, dm2 is significantly smaller than M1 (P < 0.01). However, the relative size of dm2 to M1 in matched pairs does not differ in any of the groups.

Differences should be the result of developmental timing and/or stronger environmental influences on the later forming tooth (M1). To the best of our knowledge, Smith et al.’s (1997) study is the only one that has compared deciduous and permanent dental morphology both within individuals and between fossil and recent humans. Unfortunately, it focused only on H. sapiens and their conclusion of faster growth in fossil H. sapiens was based on a single fossil H. sapiens individual (Skhul 1). Comparisons between dm2 and M1 within fossil and recent individuals using larger and more heterogeneous samples are certainly warranted. In this contribution, we compared crown outlines of dm2 and M1 within- and between-species. We made these comparisons both within the same individuals and across different individuals. We chose the crown outline for a number of reasons. First, as previously noted, Neandertals and H. sapiens differ significantly in the dm2 and M1 crown shapes; second, the shape of the crown outline reflects morphological peculiarities (enlarged hypocone and reduced metacone) previously observed in Neandertals (Bailey, 2004b; Gomez-Robles et al., 2007; Benazzi et al., 2011a); and third, using the crown outline provides us with much larger sample sizes than if we were to compare morphometric landmarks (e.g., cusp tip positions) or nonmetric traits (which often do not preserve after moderate wear). To begin, we directly examined how the shapes of dm2 and M1 within individuals compare between H. sapiens and Neandertals. We then investigated the effect of size on shape of the dm2 and M1. Neandertal dm2 and M1 are larger, on average, than those of H. sapiens (Table 1). Therefore, it is possible that the skewed shape of the M1 (and by extension the dm2) may not be a derived condition, but a predictable consequence of the larger size of the tooth. We explored this possibility by assessing allometry both within (static) and between (evolutionary) species. Along the same lines, one of the most obvious differences between dm2 and M1 is size: in a given individual the dm2 is on average 22% smaller than M1 (Table 1). Therefore, we also examined the metameric variation between dm2 and M1 to see if shape follows a predictable trajectory based on size. We asked the following questions in pursuing this research design: 1) Are dm2 and M1 crown shapes allometrically scaled in H. sapiens and Neandertals? 2) If so, what portion of the shape differences can be accounted for by allometric scaling? 3) Finally, does the scaling of the dm2 and M1 share a common trajectory and magnitude between species?

MATERIALS Our sample includes 231 specimens: 160 recent H. sapiens (RHS), 28 Upper Paleolithic H. sapiens (UPHS), 10 early H. sapiens (EHS), and 33 H. neanderthalensis

(NEA). All RHS specimens are matched dm2/M1 pairs from the same individuals (n 5 80). Of the fossil individuals, seven UPHS, three EHS, and seven NEA were matched pairs (Table 2). We chose teeth that were unworn to moderately worn (Molnar’s stages 1–5 (1971)). Severely worn teeth (Molnar’s stages 6–8) were not included because the crown outline would have been too compromised. In moderately worn teeth, interproximal wear on the mesial and/or distal aspects occasionally distorted the crown outline. In these cases, the original outlines were estimated based on the previous protocols outlined in Wood and Engleman (1988) and Bailey (2004b) by estimating the original mesial and/or distal borders based on the buccolingual extent of the wear facet and the overall contour of the tooth (Fig. 1). All estimations were made by one of us (SEB).

METHODS Without the aid of radiography or micro-computed tomography (e.g., Smith et al.’s 1997 study), it can be difficult to compare dm2 and M1 occlusal morphology within the same individual. Although dm2 and M1 may be present in the same jaw for up to 7 years (from 5–6 years until 10–12 years), within a few years after full eruption attrition can significantly obscure cusp morphology and fissure patterns, especially in archaeological and fossil specimens. Hence, by about 7 years of age, the dm2 may be so worn as to make comparisons problematic. This limits age-appropriate samples to an approximate 2-year period (age, 5–7 years) and results in small sample sizes (Paul and Bailey, 2013). We were able to maximize our sample sizes in this study by examining the outlines rather than the occlusal morphology. Although interproximal wear can alter crown outlines, even in moderately worn teeth the original shape is fairly easy to reconstruct accurately (Wood and Abbott, 1983; Wood and Engleman, 1988; Bailey, 2004b; GomezRobles et al., 2007); thus, only the most worn teeth needed to be discarded from analysis. Occlusal images of the dm2s and M1s were taken with either a Canon EOS Rebel XT digital 8 MP camera equipped with a macro lens or a Nikon D80 10.2 MP digital camera using the macro setting. Bailey et al. (2004) have shown previously that measurement error between researchers using different equipment and analysis tools was relatively low (0–5%) and not significantly different from intraobserver error. Each tooth was oriented so that the cervical border was perpendicular to the optical axis of the camera lens. The camera was leveled using a bubble device; care was also taken to make sure the scale included in each image was level. Some of the fossil teeth were imaged using three-dimensional (3D) models based on mCT scans performed by the Department of Human American Journal of Physical Anthropology

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S.E. BAILEY ET AL. TABLE 2. Sample composition

Neandertals (seven matched pairs) Cova Negra Krapina KDP 1 (45) Krapina KDP 22(D100/D185) Krapina KDP3 (D134/D189) La Ferrassie 8 La Quina H18 Roc du Marsal Arcy sur Cure 45 Kebara 1 Krapina 6 MxB Krapina 47 Krapina D186 Krapina D188 Krapina D190 Subalyuk 2 Arcy sur Cure 39 Krapina Max C Krapina Max D Krapina D101 Krapina D171 Le Fate XIII Le Moustier Monsempron 1953-1 Obi Rakhmat Petit Puymoyen St. C esaire EHS (three matched pairs)

UPHS (seven matched pairs)

15 X X X X X X X X X X X X X X X

18 X X X X X X X

X X X X X X X X X X X 7 X X X X X X X 19 X X X X X X X

9 X X X X X X X X X

Abri Pataud Kostenki 15 Lagar Velho La Madeleine St. Germain B6 St. Germain B7 Veyrier 1 Bruniquel II Die Kelders 6243 Font echevade Gough’s Cave Grotta del Fossellone Laugerie Basse Le Rois 19 Le Rois unnumbered Mladecˇ 1 Mladecˇ 2 Pesk} o Barlang St. Germain 2 Sunghir 2 Sunghir 3 RHS (80 matched pairs) Europe (Western) Asia (S. Asia, Micronesia, W. Asia, S.E. Asia) Americas (North and South) Africa (South, West, East, North)

American Journal of Physical Anthropology

UM1

3 X X X

Qafzeh 10 Qafzeh 15 Skhul 1 Dar es Soltan 1 Dar es Soltan 3 Dar es Soltan H6 Temara H7

Evolution of the Max Planck Institute for Evolutionary Anthropology, Leipzig. Both industrial and desktop microCT systems were used to scan with subsequent voxel resolutions ranging from 14 to 70 lm. The image stacks of each tooth were filtered (using a computerprogrammed macro that employs a 3D median and mean-

udm2

X X X X X X X X X X X X 80 38 8 24 10

80 38 8 24 10

of-least-variance filter) to improve tissue grayscale homogeneity and then manually segmented into enamel and dentine components using AvizoV (v6.0). The crown surface was extracted as digital surface models (.ply format) that could be properly oriented in 3D. Three-dimensional models of the mCT scans were opened in AvizoV. The R

R

ALLOMETRY, MERISM AND TOOTH SHAPE OF DM2 AND M1

Fig. 1. Moderately worn dm2 from Krapina indicating where the original outline shape has been estimated. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

tooth was oriented so that the cervical border was perpendicular to the optical axis in both mesiodistal and bucco-lingual directions (Benazzi et al., 2009). The software was used to add the appropriate scale and a screen shot was taken and saved as a .jpg file. Screen shots and photographs were opened in Adobe PhotoshopV where backgrounds were removed and contrast was adjusted so that there was a clear distinction between tooth and background. The teeth were then rotated so that they approximated anatomical position and each image was scaled to approximately the same size and resolution (300 dpi). Images of the occlusal surface of the M1s and dm2s were imported in Rhino 4.0 Beta CAD environment (Robert McNeel & Associates, Seattle, WA) and aligned to the xy-plane of the Cartesian coordinate system to analyze crown outlines. The crown outline was manually digitized for each tooth using the spline function, and then oriented with the lingual side parallel to the x-axis. Outlines were first centered superimposing the centroids of their area and then represented by 24 pseudolandmarks obtained by equiangularly spaced radial vectors out of the centroid (Benazzi et al., 2011a: Fig. 1). The first radius is directed buccally and parallel to the yaxis of the Cartesian coordinate system. Size information from the centered and oriented outlines was removed with a uniform scaling of the pseudolandmark configurations to unit centroid size (Benazzi et al., 2011b, 2011c, 2012). As emphasized by Benazzi et al. (2012), the procedure followed differs from a proper generalized Procrustes analysis because rotation and translation have been constrained by anatomical considerations. After being scaled to unit centroid size, the shape coordinates 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 between the positions of corresponding pseudolandmarks) between mean shapes were carried out to test the statistical significance of molar (dm2 and M1) shape difference within and between Neandertals and H. sapiens (which includes EHS, UPHS, and RHS), and between tooth classes. For each permutation test, speciR

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mens were randomly reassigned with respect to group, either tooth class or species, and the Procrustes distance between the new group means was then computed (Good, 2000; Zelditch et al., 2004). A principal component analysis (PCA) of the matrix of shape coordinates was carried out to explore the pattern of morphological variation across the dm2 and M1 samples. Shape variation related to size (allometric changes) was first investigated by Pearson product–moment correlation coefficient (r) of shape variables (PCs) on the logarithm of crown base area and cusp base areas. SigmaScan Pro was used to measure crown base area and individual cusp areas (protocone, paracone, metacone, and hypocone). Images were first calibrated using the scale in each photograph and then areas were measured using the trace function. Each cusp was considered independently to evaluate which of them drives the allometric changes, and then multivariate regression of shape variables (using both all the PCs and only the first three PCs) on the most informative cusp was carried out to compute the interspecific allometric trajectory across the dm2s-M1s morphospace. The null hypothesis of shared allometric trajectory of the groups was assessed by measuring the angle between allometric vectors, calculated as the dot product of regression coefficients (Cardini and Elton, 2007), whereas differences in vector magnitude (length) were computed as the absolute difference in vector lengths. The statistical significance of observed vector angle and magnitude was determined using a permutation test (n 5 1,000), where the two groups were combined and molars (dm2s and M1s) were randomly reassigned to species before computing the angular differences (Good, 2000; Zelditch et al., 2004). Finally, two-block partial least squares (2B-PLS) analysis (also called singular warp [SW] analysis when applied to Procrustes coordinates (Rohlf and Corti, 2000; Bookstein et al., 2003)) was used to explore the patterns of covariation between dm2 and M1 crown outlines in a subsample of the 194 specimens, representing 97 individuals for which both the dm2 and the M1 were available: 80 RHS, 7 UPHS, 3 EHS, and 7 NEA. So as to compare only the patterns of covariation, irrespective of group mean differences and allometric differences (Mitteroecker and Bookstein, 2008; Mitteroecker et al., 2012), we first centered each species removing the within-group mean (independently for dm2s and M1s), and then regressed out size (logarithm of the most important cusp) from the shape coordinates to remove allometric shape variation. The noncentered shape coordinates were then projected on the computed PLS vectors to produce the SW scores, which then showed mean differences, if they existed. A permutation test was used to assess the statistical significance of the Pearson product–moment correlation coefficient (r) between the first pair of SWs (SW1s). The data were processed and analyzed through software routines written in R (R Development Core Team, 2012).

RESULTS Basic statistics for crown sizes of dm2s and M1s and relative size of dm2 to M1 in matched pairs are reported in Table 1. Within individuals, the dm2 is always smaller than the M1, and differences between the two teeth are highly significant. Neandertals also have significantly larger dm2 and M1 compared to RHS and UPHS but not EHS. Interestingly, the relative size of the dm2 (i.e., American Journal of Physical Anthropology

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S.E. BAILEY ET AL. TABLE 3. Between-tooth class Procrustes distances N-M1 2

N-dm EHS-dm2 UPHS-dm2 RHS-dm2 HS-dm2

EHS-M1

UPHS-M1

RHS-M1

HS-M1

a

0.0157

0.0236 0.0104 0.003 0.0026

TABLE 4. Within-tooth class Procrustes distances (M1) N-M1 EHS-M UPHS-M1 RHS-M1 HS-M1

N-dm2

EHS-dm2

UPHS-dm2

0.0454a 0.0437a 0.0436a 0.0435a

0.0141 0.0152

0.0089

2

N, Neandertals; EHS, early H. sapiens; UPHS, Upper Paleolithic H. sapiens; RHS, recent H. sapiens; HS 5 EHS 1 UPHS 1 RHS. a Significant difference at P < 0.05.

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TABLE 5. Within-tooth class Procrustes distances (dm2)

EHS-M1

UPHS-M1

0.025a 0.017a

0.0113a

a

0.04 0.0514a 0.0435a 0.0444a

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

dm2/M1) appears to be quite stable and does not differ significantly among Neandertals and H. sapiens groups. Permutation tests (Table 3) show that between tooth classes (dm2 against M1), Procrustes distances were significantly different in Neandertals (q 5 0.0157, P 5 0.033), but not in H. sapiens, either when the subgroups were considered separately (RHS: q 5 0.003, P 5 0.87; UPHS: q 5 0.0104, P 5 0.576; EHS: q 5 0.0236, P 5 0.246) or when they were combined (q 5 0.0026, P 5 0.894). With regard to within-tooth class Procrustes distances (Table 4), M1s were significantly different for all between-groups (Neandertals and H. sapiens) and subgroups (RHS, UPHS, and EHS) comparisons (P < 0.03). For the dm2 (Table 5), significant differences were observed only between Neandertals and H. sapiens (P < 0.001), but not between H. sapiens subgroups (RHS– UPHS: q 5 0.0089, P 5 0.624; RHS–EHS: q 5 0.0152, P 5 0.375; UPHS–EHS: q 5 0.0141, P 5 0.625). Results of the shape–space PCA of the dm2s and M1s are shown in Figure 2. The first three PCs account for about 72% of the total variance. Neandertals and H. sapiens differ significantly (permutation test, n 5 1,000) along PC1 (46.6%, P < 0.001), which accounts for shape variation related to hypocone expansion and skewed outline shape (positive PC1), and hypocone reduction with mesiodistal compression of the outline (negative PC1). Neandertals have generally positive PC1 scores. It is worth noting a significant trend toward higher PC1 values for M1s than dm2s (P < 0.001), both for Neandertals and H. sapiens, although the trend is stronger in the former. Shape differences along PC2 (13.7%) are mainly driven by the expansion of the metacone and reduction of the protocone (positive PC2), and expansion of both the hypocone and the protocone, with concomitant reduction of the metacone (negative PC2). No significant differences were observed between Neandertals and H. sapiens for PC2 (P 5 0.092), but in H. sapiens M1s significantly differ from dm2s in having lower PC2 scores (P < 0.002). Correlation tests between the PCs and the crown base area emphasize that PC1 is more correlated with size (r 5 0.413, P < 0.001) than the other PCs. When the correAmerican Journal of Physical Anthropology

N-dm EHS-dm2 UPHS-dm2 RHS-dm2 HS-dm2

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

lation is carried out using individual cusp base areas, it is evident that PC1 is more strongly correlated with hypocone base area (r 5 0.559, P < 0.001) than with protocone (r 5 0.237, P 5 0.001), paracone (r 5 0.25, P < 0.001), or metacone (r 5 0.359, P < 0.001) base areas. Therefore, the allometric trajectory across the dm2s–M1s morphospace for the two groups (Neandertals and H. sapiens) was computed by multivariate regression of shape variables on hypocone base area (Fig. 2). When the two groups are combined, this analysis reveals a small but significant allometric effect that accounts for 16.2% of the total morphological variance in dm2 and M1 crown shape. However, when the two groups are considered separately, the allometric effect explains a large fraction of variance in Neandertals (70.2%), but only a small portion of variance in H. sapiens (11.5%). Although the allometric trajectories are not parallel, angular differences between Neandertal and H. sapiens dm2/M1 allometric vectors failed to reach statistical significance (58 , P 5 0.065). The magnitude of the interspecies allometric variation, however, does differ significantly between the two groups (P < 0.001), with the vector being larger in Neandertals (0.077) than in H. sapiens (0.027). Results did not change when the first three PCs were considered for multivariate regression analysis, both for angle (44 , P 5 0.149) and magnitude (P < 0.001). Such results suggest that we cannot reject the null hypothesis of similar allometric trajectory from dm2s to M1s for Neandertals and H. sapiens. Nevertheless, the allometric vectors are of significantly different magnitudes (Fig. 2). We undertook a permutation test (n 5 1,000) of 34 randomly selected recent modern humans (17 M1/dm2 pairs) to investigate the effect of uneven sample sizes on the above allometric trends. No significant changes in the angular differences between Neandertal and H. sapiens dm2/M1 allometric vectors were found when the smaller subsample of RHS was used (51 , P 5 0.39). Considered separately, within-species allometric trajectories of dm2s and M1s (based on the first three PCs) were not significantly different, either in Neandertals (11 , P 5 0.885) or in H. sapiens (59 , P 5 0.454). Neither were significant differences observed within-tooth class allometric trajectories of Neandertal and H. sapiens M1s (101 , P 5 0.134) and of Neandertal and H. sapiens dm2s (59 , P 5 0.522) (Fig. 3). With regard to the 2B-PLS analysis of the 97 individuals (194 dm2s and M1s belonging to the same individuals; Fig. 4), the first pair of SWs explains about 41% of the covariance between the shape coordinates of the dm2 and M1 crown outlines. The analysis reveals a significant correlation between M1 and dm2 crown shape in our hominin sample (r 5 0.62, P < 0.001). This result emphasizes that when a M1 crown shows marked hypocone expansion and skewed crown shape (negative SW-

ALLOMETRY, MERISM AND TOOTH SHAPE OF DM2 AND M1

7

Fig. 2. Shape–space PCA plots of Neandertals and H. sapiens (EHS, early H. sapiens; UPHS, Upper Paleolithic H. sapiens; RHS, recent H. sapiens) dm2 and M1 crown outlines. The deformed mean outline in the four directions of the PCs is drawn at the extremity of each axis. The allometric trajectory vectors across the dm2s–M1s morphospace are shown for Neandertals (in red) and H. sapiens (in black). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

M1 in Fig. 4), or hypocone reduction and general subsquare outline shape (positive SW1 M1 in Fig. 4), the same trend tends to be equally observed in the dm2 crown (negative and positive SW1-dm2, respectively; Fig. 4), albeit with a slightly lower expression of these features.

DISCUSSION Our results confirm the previous findings that the crown outlines of both the dm2 and the M1 of Neandertals are significantly different from those of H. sapiens (Bailey, 2004b; Gomez-Robles et al., 2007; Benazzi et al., 2011a; Bailey et al., 2013). As it might be expected given their overall similarity, in both species the shape of the dm2 mirrors that of the M1. The finding in this study that the shape (dm2 or M1) is most highly correlated with hypocone size, is in line with earlier studies showing the Neandertal M1 shape results from a protruding and relatively larger hypocone coupled with a relatively smaller metacone (Bailey, 2004b; Gomez-Robles et al., 2007; Benazzi et al., 2011a; Quam et al., 2009). In contrast, in H. sapiens both the dm2 and the M1 possess a relatively smaller hypocone coupled with a relatively larger metacone. Our comparison of dm2 with M1 revealed that in both species there is a trend for the M1 to possess a more skewed outline relative to the dm2, and this is reflected by the M1 possessing a higher score for PC1 than the dm2 (Figs. 2 and 3). The magnitude of this trend is stronger in Neandertals than in H. sapiens: shape differences between the two teeth were only significant in the

former, in which the skew of the M1 is especially exaggerated. The analysis of the effect of size on shape revealed that this skewed outline is partially related to tooth size although the allometric effect is much stronger in Neandertals than in H. sapiens. In both samples, the larger M1 was more skewed than the smaller dm2. Similarly, the larger (on average) Neandertal M1s are more skewed than the smaller (on average) M1 of H. sapiens. A previous morphometric study of M1 shape (GomezRobles et al., 2007) also found a significant allometric effect although it was much smaller (3.02%) than that we found in this study. In contrast to our results, Gomez-Robles and colleagues found that smaller molars had a tendency to have a more skewed shape, whereas larger molars tended to have a less skewed shape. We believe the differences between our study and the study by Gomez-Robles et al. are the result of different sample compositions. Gomez-Robles et al. (2007) assessed allometry across a wide range of hominin taxa (Paranthropus, Australopithecus, and Homo), whereas we examined two closely related Homo taxa. Therefore, it is difficult to decide whether differences among large- and smalltoothed individuals found by Gomez-Robles et al. are the result of allometry or whether the extremes on both ends (H. sapiens vs. Paranthropus) were driving the results (see also Martinon-Torres et al., 2006: p 531). In this study, we have avoided any confounding intergeneric factors by examining two closely related species that are more similar in tooth size. Based on our results, it may be tempting to conclude that the difference between upper molar shapes of H. sapiens and Neandertals is the predicted result of size American Journal of Physical Anthropology

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Fig. 3. Shape–space PCA plots of Neandertals and H. sapiens (EHS, early H. sapiens; UPHS, Upper Paleolithic H. sapiens; RHS, recent H. sapiens) dm2 and M1 crown outlines. Separate allometric trajectories for dm2 and M1 are shown for Neandertals (in red) and H. sapiens (in black). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Fig. 4. Scatterplot of the first singular axes obtained in the 2B-PLS analyses, which explains about 41% of the total covariance. The outline shape corresponding to the minimum and maximum values on each axis is provided below x-axes (for M1s, continuous line) or to the left of y-axes (for dm2s, dashed line). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

American Journal of Physical Anthropology

differences. However, there is a good deal of overlap in size of both M1 and dm2 between Neandertals and H. sapiens (Table 1), and it is clear that the largest H. sapiens teeth do not necessarily exhibit the most Neandertal-like (i.e., skewed) morphology. For example, tooth sizes of Neandertals and EHS do not differ significantly (Table 1), but their tooth shape does (Table 4). Moreover, our Aterian sample has the largest upper molars of any Middle–Late Pleistocene Homo (including Neandertals). Yet, the M1s do not show the predicted hyper-skewed shape (Fig. 2). Hence, we are left with the fact that Neandertals have dm2 and M1 that are significantly larger and significantly more skewed than they are in H. sapiens. In general, M1s are significantly larger than dm2 and are also significantly more skewed (but only in Neandertals). Although the allometric trajectories of the two species do not differ significantly for either dm2 or M1, they are dramatically different (nearly opposite, Fig. 3); and there appears to be different patterns for molar variation between Neandertals and H. sapiens. Although we found that the difference in sample sizes (H. sapiens vs. Neandertals) did not significantly affect differences in allometric vectors, we cannot rule out that with a larger Neandertal sample the differences between the two species would become significant. However, it may also be worth considering other factors that could be involved in the distinctive shapes of the Neandertal dm2 and M1. One possibility (not tested here) is that the pace of growth and/or developmental timing has an effect on upper molar crown shape. Recent studies have shown that Neandertal postcanine teeth grew faster than those of H. sapiens (Smith et al., 2007a,b). We also know that

ALLOMETRY, MERISM AND TOOTH SHAPE OF DM2 AND M1 1

Neandertal M s have cusps that are significantly more closely spaced compared to H. sapiens (Bailey, 2004b; Gomez-Robles et al., 2007). The pattern cascade model (Jernvall, 2000; Jernvall and Jung, 2000) suggests that cusp spacing is correlated with cusp size and cusp number. Therefore, it is possible that the more closely spaced cusp tips (e.g., enamel knots) in Neandertals have allowed for stronger expression of the hypocone. As relative hypocone size strongly influences shape (especially in Neandertals; this study), it is likely that cusp spacing is directly influencing the differences between Neandertal and H. sapiens upper molar shapes. A test of this would be to investigate whether cusp spacing in dm2 also differs significantly between Neandertals and H. sapiens. Differences in cusp spacing may also contribute to the shape differences between dm2 and M1. If so, we would predict the M1 to have more closely spaced cusps than dm2. The longer growth period of the M1 (in both Neandertals and H. sapiens) may also be found to influence its final shape. Future comparisons of relative cusp areas and morphometric variables (cusp spacing) as well as comparisons of growth between dm2 and M1 both within- and between-species will go far in resolving this issue (Bailey, in prep).

A FINAL NOTE ABOUT THE “PRIMITIVE” NATURE OF DM2 As dental meristic elements have been thought to represent sequential phases of the development of the same basic tooth (Dahlberg, 1945; Butler, 1956; Kraus and Jordan, 1965; Butler, 1967a, 1967b, 1971; Sofaer et al., 1972; Saunders and Mayhall, 1982; Smith et al., 1987; Smith, 1989), it is tempting to see the deciduous second molar and permanent first molar as representing different stages of the same ontogenetic process. If this is so, one may wish to apply the ontogenetic method for determining trait polarity (Rieppel, 1990), and view the morphology of the deciduous second molar as representing the primitive condition of the permanent first molar. For example, Smith et al. (1997) found that cusp spacing of the RHS lower deciduous second molar (dm2) resembled EHS (Skhul 1) dm2 and lower first molar (M1) more than it did the RHS M1. They attributed the similarities between the dm2 and the M1 of fossil H. sapiens and the dm2 of RHS to faster growth of the former (dm2) compared to the latter (M1). By extension, they hypothesized that fossil H. sapiens grew faster than RHS and that the deciduous second molar preserves the “primitive” condition (i.e., faster growth) for our lineage. “On the basis of this assumption, we infer that the resemblance found between the Skhul DM2 and M1 and the recent DM2 may indicate a similar growth pattern and that the slow growth rate for the recent permanent molar relative to DM2 may be a relatively new phenomenon” (page 293) Based on the Procrustes distances computed in this study, this hypothesis is only moderately supported. Although we did find some support for the primitive nature of dm2 shape in RHS (nonsignificant Procrustes distances among fossil and RHS samples), our results also showed that in both fossil and RHS the shape of the dm2 was not significantly different from the M1. In fact, it appears that the primitive (more square shape) is shared between M1 and dm2. In contrast, the shape of

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the dm differed significantly between Neandertals and all H. sapiens groups. The distinct separation of the dm2 of Neandertals and H. sapiens (see also Benazzi et al., 2011b), with the dm2 mirroring the derived shape of the M1, suggests that the dm2 shape of Neandertals is also derived, rather than a primitive retention. A recent study of dm2 shape provides further support for the derived state of the Neandertal dm2 and primitive state of the H. sapiens dm2 (Bailey et al., in review). When discussing primitive and derived characters, it is important to remember that these terms are relative. A trait that is primitive for a lineage may not be primitive for the entire clade. Hence, although the dm2 shape of RHS may be primitive (has basically not changed since the origin of our lineage), it does not mean that the dm2 (generally speaking) represents the primitive condition for the Homo clade. Indeed, the Neandertal dm2 possesses a derived shape similar to (but not as pronounced as) that in the M1. Hence, although dm2 of H. sapiens does retain a higher frequency of certain archaic traits (e.g., Dryopithecus molar pattern, cusp 7) than does the M1, we believe that it is inappropriate to presume that the dm2 and deciduous elements, in general, provide us with “window” into trait polarity. Indeed, nearly 50 years ago von Koenigswald (1967) made the same point, stating: “There are deciduous dentitions with primitive, or ‘conservative,’ traits, whereas there are other deciduous dentitions that are prophetic, or ‘progressive’. . .” (page 779). In light of our results, we suggest the use of the outgroup method rather than an ontogenetic model, for determining trait polarity.

ACKNOWLEDGMENTS The authors thank Philipp Mitteroecker and Philipp Gunz for important comments and methodological suggestions. The authors also thank Claudia Astorino for assistance with image processing. The authors thank Kathleen Paul and Caroline Souday who gathered images of some of the recent human groups under the supervision of SEB. Data collection was supported by the LSB Leakey Foundation and National Science Foundataion (SEB).

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