Journal of Evolution 118 (2018) 14e26

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Dental topography and the diet of naledi

* Michael A. Berthaume a, b, , Lucas K. Delezene c, d, Kornelius Kupczik a a Max Planck Weizmann Center for Integrative Archaeology and Anthropology, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, Leipzig, 04103, Germany b Department of Anthropology, Durham University, Dawson Building, South Road, Durham, DH1 3LE, United Kingdom c Department of Anthropology, University of Arkansas, 330 Old Main, Fayetteville, AR, 72701, USA d Evolutionary Studies Institute, University of the , 1 Jan Smuts Avenue, Braamfontein 2000, Johannesburg, article info abstract

Article history: Though late Middle Pleistocene in age, Homo naledi is characterized by a mosaic of -like Received 27 October 2017 (e.g., curved fingers, small brains) and Homo-like (e.g., elongated lower limbs) traits, which may suggest Accepted 8 February 2018 it occupied a unique ecological niche. Ecological reconstructions inform on niche occupation, and are particularly successful when using dental material. Tooth shape (via dental topography) and size were quantified for four groups of South African Plio-Pleistocene hominins (specimens of Australopithecus Keywords: africanus, robustus, H. naledi, and Homo sp.) on relatively unworn M2s to investigate Australopithecus africanus possible ecological differentiation in H. naledi relative to taxa with similar known geographical ranges. South African Homo H. naledi has smaller, but higher-crowned and more wear resistant teeth than Australopithecus and Dental topography Paranthropus. These results are found in both lightly and moderately worn teeth. There are no differences Dietary reconstruction in tooth sharpness or complexity. Combined with the high level of dental chipping in H. naledi, this suggests that, relative to Australopithecus and Paranthropus, H. naledi consumed foods with similar fracture mechanics properties but more abrasive particles (e.g., dust, grit), which could be due to a di- etary and/or environmental shift(s). The same factors that differentiate H. naledi from Australopithecus and Paranthropus may also differentiate it from Homo sp., which geologically predates it, in the same way. Compared to the great apes, all hominins have sharper teeth, indicating they consumed foods requiring higher shear forces during mastication. Despite some anatomical similarities, H. naledi likely occupied a distinct ecological niche from the South African hominins that predate it. © 2018 Elsevier Ltd. All rights reserved.

1. Introduction Little is known about the ecology of the recently discovered hominin Homo naledi (Berger et al., 2015, 2017; Hawks et al., 2017). Ecological reconstructions help clarify niche partitioning, and Though Middle Pleistocene (236e335 ka) in age (Dirks et al., 2017), some of the most successful hominin reconstructions have relied it resembles species of Australopithecus by evincing a short stature, on dental remains (e.g., Grine et al., 2012; Henry et al., 2012; small body mass, and small brain, both absolutely and relative to Sponheimer et al., 2013). Dental differences (e.g., absolute and body size (Garvin et al., 2017). Small brains and bodies indicate relative tooth size, dental proportions, dental topography, absolute differing energetic requirements and home ranges compared to and relative enamel thickness) among hominin taxa are often cited other species of Middle Pleistocene Homo (Anton et al., 2014). to reflect dietary shifts, but can also reflect environmental or a Further, curved fingers and aspects of shoulder morphology sug- combination of environmental and dietary shifts (Lucas et al., 2008; gest significant levels of climbing (Kivell et al., 2015; Feuerriegel Ungar and Sponheimer, 2011). For example, increases in aridity can et al., 2017), which could point towards an Australopithecus-like lead to a decrease in fruit availability, a change in food mechanical pattern of resource exploitation (Perez-P erez, 1988; Pruetz, 2006) properties, and/or an increase in dust/grit consumption (Onoda for H. naledi. Yet, similar to Homo and unlike Australopithecus, the et al., 2011). lower limb is elongated (Marchi et al., 2017), sexual size dimor- phism is minimal (Garvin et al., 2017), and the postcanine teeth are absolutely small (Berger et al., 2015; Hawks et al., 2017). In these regards, H. naledi appears to be a late surviving member of the * Corresponding author. E-mail address: [email protected] (M.A. Berthaume). genus Homo. This begs the question of whether H. naledi occupied https://doi.org/10.1016/j.jhevol.2018.02.006 0047-2484/© 2018 Elsevier Ltd. All rights reserved. M.A. Berthaume et al. / Journal of Human Evolution 118 (2018) 14e26 15 an ecological niche more like Australopithecus, other species of Arsuaga, 2017). The C4 and dental microwear signatures make a Middle Pleistocene Homo, or neither. shift towards bulk feeding less likely, as bulk feeding tends to Resolving this issue is complicated due to the minimal faunal manifest in higher C4 values and more scratches/less pits. remains associated with the more than 1550 and 131 H. naledi Compared to P. robustus, Homo sp. has smaller teeth with absolutely fossils from the Dinaledi and Lesedi chambers, respectively, and the and relatively thinner enamel (Skinner et al., 2015), which, given lack of tools associated with this species (Berger et al., 2015; Dirks that the two taxa lived in the same environment, points towards et al., 2015, 2017; Hawks et al., 2017). The paucity of these data dietary differentiation, possibly due to different food processing inhibits robust reconstructions of the H. naledi paleoenvironment methods (e.g., extraoral food processing with tools and/or cooking and its pattern of resource exploitation. In this paper, we investi- foods in Homo; Wrangham, 2009; Zink et al., 2014). Functional gate the dietary ecology of H. naledi by quantifying tooth shape and studies have produced contradictory results, suggesting that A. contextualize the results by comparing them to three other groups africanus was both better and worse adapted for consuming hard, of South African hominins: Australopithecus africanus, Paranthropus brittle food items than P. robustus (Spears and Crompton, 1994; robustus, and Homo sp. (i.e., Stw 80, SK 15, Cave of Hearths Berthaume et al., 2010). Although disparities can arise depending ), all of which are presumed to predate the remains of on the method used and how the results are interpreted, all studies H. naledi from Rising Star. point toward ecological differentiation among South African taxa.

1.2. Dental topography 1.1. Dental paleoecological evidence for Plio-Pleistocene hominins in South Africa A popular method for quantifying tooth shape, dental topo- graphic analysis, is used here to contextualize potential ecological Between 3.0 and 1.5 Ma, there were at least four hominin taxa in differentiation in H. naledi (Zuccotti et al., 1998; Evans, 2013). South Africa, and ecological reconstructions for A. africanus, Dental topography is “a method of quantifying and representing 2.5 P. robustus, , and Homo sp. indicate some or 3D whole tooth shape with a single metric” (Berthaume, 2016a: niche partitioning (Grine et al., 2012; Henry et al., 2012). During this 680), and has successfully been used to correlate tooth shape to diet time, the environment in South Africa changed from more closed (Ungar, 2004; King et al., 2005; Godfrey et al., 2012; Ledogar et al., and mosaic to more open and arid (e.g., Vrba, 1975, 1985; Reed, 2013; Winchester et al., 2014; Berthaume and Schroer, 2017). 1997; Lee-Thorp et al., 2007). Carbon isotope data from dental Originally developed using geographic information systems (GIS) enamel reveal dietary overlap in these hominins and consumption technology (Zuccotti et al., 1998; Ungar and Williamson, 2000), it of C resources (Lee-Thorp et al., 1994; Sponheimer and Lee-Thorp, 4 has since come to encompass several non-GIS specific methods 1999; Sponheimer et al., 2005, 2013; Grine et al., 2012), with the (Evans, 2013). Besides inferring dietary ecology, dental topography exception of A. sediba (see Henry et al., 2012). In A. africanus and has also been used to predict enamel surface morphology from the Homo sp., dental microwear textures show a large range in shape of the enamel-dentine junction (Skinner et al., 2010; Guy anisotropy (epLsar ) and low range in complexity (Asfc) due to a 1.8 et al., 2015), to investigate evolutionary pressures, such as niche high density of scratches and a low density of pits. This has been partitioning (Boyer et al., 2012; Godfrey et al., 2012; Berthaume and interpreted as indicating consumption of ‘tough’, mechanically Schroer, 2017), and to describe and assign a fossil to a new challenging foods. The opposite is found in A. sediba and some species (Boyer et al., 2012). The relationship between tooth shape specimens of P. robustus, indicating occasional consumption of and food item breakdown have additionally been investigated ‘hard’ foods (Scott et al., 2005; Ungar and Scott, 2009; Ungar and (Thiery et al., 2017a, 2017b), but how foods break down during Sponheimer, 2011; Henry et al., 2012; Ungar et al., 2012).1 It has mastication is not yet fully understood, and the proposed cate- been argued that more complex microwear textures could also be a gories (e.g., crushing, grinding) need to be better defined from a product of increased quartz consumption, due to living in a more fracture mechanics standpoint before this classification system can arid environment (Lucas et al., 2013; Schulz et al., 2013; Merceron be used (Berthaume, 2016b; Thiery et al., 2017b). et al., 2016)dmeaning that the observed differences between A. The first metrics to reliably quantify tooth shape and relate it to africanus and P. robustus could be due to greater dust or grit con- dietary ecology, shearing ratio and shearing quotient, established sumption, as a result of increased aridity (Vrba, 1975, 1985; Reed, that teeth with relatively longer shearing crests were more efficient 1997; Lee-Thorp et al., 2007). However, a broad analysis of extinct at masticating fibrous and chitinous foods in small hominins and bovids and experimental work on dust suggests that (Sheine and Kay, 1977, 1982). A major drawback of this approach is increasing dust and/or grit in the diet is unlikely to explain the that shearing crests can be measured only on unworn teeth with interspecific and regional differences observed in hominin micro- defined shearing crests. Dental topography overcomes these limi- wear (Merceron et al., 2016; Ungar et al., 2016). As P. robustus and tations and can be used to quantify dental morphologies at all wear Homo sp. fossils have been recovered from the same stratigraphic stages (Ungar and M'Kirera, 2003; Winchester et al., 2014). We units at and (e.g., Grine et al., 2009; Moggi- employ four dental topographic metrics in the South African Cecchi et al., 2010), differences in dental microwear between hominins: orientation patch count rotated (OPCR), Dirichlet normal them are likely due to diet. energy (DNE), relief index (RFI) and ambient occlusion (PCV, Assessing tooth size and structure, P. robustus has relatively portion de ciel visible or ‘portion of visible sky’). Orientation patch larger molars with thicker enamel than many other hominins, count rotated is used to quantify occlusal complexity (Evans et al., possibly indicating an adaptation towards bulk feeding (i.e., the 2007). From a functional perspective, it quantifies the number of consumption of large amounts of poor quality foods), high bite ‘tools’ (e.g., cusps, crests, crenulations, and cutting edges) on the force production, and/or consumption of more dietary abrasives tooth's surface: a tooth with more tools is more efficient at chewing (McHenry, 1984; Madden, 2015; Skinner et al., 2015; Ruiz and foods with structural fibers and has a higher OPCR value. Dirichlet normal energy is a measure of surface curvature, and is used to quantify tooth sharpness, with sharper teeth having higher DNE 1 The definitions of ‘tough’ and ‘hard’ foods do not always align with those in values (Bunn et al., 2011). Unlike other measures of curvature (e.g., engineering/materials science, where tough items absorb large amounts of energy per unit volume, and hard ones resist plastic deformation at their surface curvature in Guy et al., 2013), DNE does not differentiate between (Berthaume, 2016b). convexities and concavities (i.e., positive and negative curvatures). 16 M.A. Berthaume et al. / Journal of Human Evolution 118 (2018) 14e26

However, it is strongly positively correlated to shearing quotient for accession numbers). Lower second molars were chosen and shearing ratio in unworn teeth, indicating that it is a good because: 1) they are morphologically highly (although not exclu- measure of positive tooth curvature (Bunn et al., 2011; Winchester sively) representative of the postcanine dentition (Kay, 1975; et al., 2014). Unlike shearing quotient and shearing ratio, DNE can Sheine and Kay, 1977); 2) the relationship between M2 shape and be used for teeth with a variety of morphologies in a variety of wear diet in is well established (e.g., Boyer, 2008; Godfrey et al., stages (Pampush et al., 2016). Depending on the surface cropping 2012; Ledogar et al., 2013; Winchester et al., 2014); and 3) dietary method used (i.e., the entire crown or just the portion of the crown signatures are stronger in mandibular than maxillary teeth in superior to the lowest point on the talonid basin), relief index (RFI) dental topographic analyses (Allen et al., 2015). This does not imply quantifies relative crown and/or height. High-crowned/ other postcanine teeth hold no dietary signatures (e.g., Kay, 1975, cusped teeth have higher RFI values, while teeth with lower 1981; Sheine and Kay, 1977, 1982; Berthaume, 2014; Winchester crowns/cusps have lower RFI values (Ungar and M'Kirera, 2003; et al., 2014; Allen et al., 2015). The sample of Homo sp. includes Boyer, 2008). Finally, ambient occlusion, a relatively new dental fossils from Swartkrans (i.e., SK 15), Member 5 West topographic metric, quantifies the likelihood of tooth wear (i.e., Stw 80), and the mandible from the Cave of Hearths that have (Berthaume, 2016a). Ambient occlusion is a method for making 3D been referred to as /. The Cave of images appear more realistic by approximating the amount of Hearths mandible is poorly dated, but recovered from ambient lighting that would be shining across the surface. levels (Herries, 2011). It was suggested that this mandible could Measured from above the occlusal surface, a point with higher belong to H. naledi (Berger et al., 2017), but it differs from H. naledi ambient occlusion, or PCV, will be more likely to contact a food in premolar and molar crown morphology (L.K.D., pers. obs.), and item/opposing tooth during a masticatory cycle than a point with plots out separately from H. naledi in most of our analyses. It is lower PCV. Consequently, areas of the tooth with higher PCV values likely younger than either the Swartkrans or Sterkfontein Homo have an increased probability of wearing during a masticatory cy- material included in this study and may represent Homo rhode- cle. Portions of the tooth responsible for food item fracture (e.g., siensis/ (e.g., Tobias, 1971; Kuman and Clarke, cusps and crests) tend to have higher PCV values, while areas 2000; Herries and Shaw, 2011). Due to small sample size, two responsible for trapping/stabilizing the food item and increasing possible antimeres were included for H. naledi; in particular, U.W. dental longevity (e.g., basins, and the sides of the crown, respec- 101e507 and U.W. 101e145 are likely antimeres, and U.W. 101e377 tively) tend to have lower values (Fig. 1; Berthaume, 2016a). When and U.W. 101e789 have been suggested to be antimeres (L.K.D., all PCV values are averaged over the surface, teeth with lower mean pers. obs.), although the former is 12.67% smaller than the latter PCV values are less likely to experience large levels of wear during (128.334 mm2 vs. 146.955 mm2, quantified through outline area; mastication and are, therefore, more wear resistant. In addition to Boyer, 2008). No antimeres were used for A. africanus or P. robustus, the dental topographic metrics, tooth size, measured via projected and no antimeres were present for Homo sp. cross-sectional area (Boyer, 2008), was quantified, as this measure is correlated to diet in primates. 2.2. Surface digitization

2. Materials and methods Digital representations of the teeth were created using a BIR Actis 300/255 FP, SkyScan 1172, or a Nikon Metrology XTH 225/320 2.1. Sample microtomography (microCT) scanner at resolutions of 14e91 mm (only four teeth are at a resolution of 91 mm, all other teeth are at Out of a total of 102 mandibular second molars available from resolutions of 14e36 mm; see SOM Table S2 for resolutions). CT eight South African fossil hominin-bearing sites, 43 relatively un- scans were processed in Avizo 8.1 (FEI, Hillsborough, USA) by worn teeth with well-preserved enamel caps were selected for thresholding, removing any matrix or bone touching the outer analysis (A. africanus ¼ 16, P. robustus ¼ 16, H. naledi ¼ 8, Homo surface of the enamel cap, using the ‘smooth labels’ command sp. ¼ 3; see Supplementary Online Material [SOM] Tables S1 and S2 (size ¼ 3, 3D volume), and generating surfaces (smoothing type: existing weights). Surfaces files were imported into Geomagic Studio 2013 (3D Systems, Morrisville, USA), where the outer surface of the enamel cap was isolated and edited (e.g., smoothed, recon- structed, and/or erasing cracks; SOM Table S2). When necessary and possible, portions of missing enamel along the cervical margin were repaired, and teeth were cropped. Two surface cropping methods are commonly used for dental topography, using the entire enamel cap (EEC) or the portion of the enamel cap superior to the lowest point on the occlusal basin (BCO). BCO is popular because it is not always possible to mold or scan the entire tooth or because of enamel chipping along the cervical margin (Zuccotti et al., 1998; Ungar and Williamson, 2000; M'Kirera and Ungar, 2003; Ungar and M'Kirera, 2003; Dennis et al., 2004; King et al., 2005; Evans et al., 2007; Godfrey et al., 2012; Berthaume and Schroer, 2017). Entire enamel cap was introduced in Boyer (2008) because there were taxa for which the BCO could not be reliably employed. The EEC method is advantageous as it considers whole tooth shape, providing information about tooth Figure 1. 2D image of light shining from the superior direction onto the occlusal shape not responsible for food item breakdown that is related to surface of the tooth. Portions of the tooth that are more exposed to ambient light (i.e., diet (e.g., relative crown height), but requires 3D scans. The BCO high exposure) are more likely to come in contact with food, grit, and/or an opposing method is advantageous as it attempts to isolate portions of the tooth during mastication, making them more likely to experience wear than areas less exposed to ambient light (i.e., low exposure). Teeth that are less exposed to ambient teeth responsible for food item breakdown and can be done with light have a lower PCV score and are more wear resistant. both 2.5 and 3D scans, as the cervix is not always imaged in 2.5D M.A. Berthaume et al. / Journal of Human Evolution 118 (2018) 14e26 17 scans. Previous studies have reported no significant differences in averaging the scores from across the five cusps. Tooth wear was dental topographic values due to cropping method (Bunn et al., scored using a combination of photographs of the fossils and the 2011; Godfrey et al., 2012; Prufrock et al., 2016), but have suffered surface files of the teeth. from small sample sizes. All teeth were subjected to both the ECC and BCO to determine if the two cropping methods produced sta- 2.5. Statistical analyses tistically different results. Edited tooth surfaces were reimported into Avizo, simplified Statistical analyses were run in RStudio using R v3.2.3 on the down to 10,000 and 20,000 triangles, and smoothed (100 itera- 10,000 EEC, 20,000 EEC, 10,000 BCO, and the 20,000 BCO separately tions, lambda ¼ 0.6; Boyer, 2008; Bunn et al., 2011; Winchester (R Development Core Team, 2015). A two-way ANOVA was run to et al., 2014). Triangle counts of 10,000 are standard for DNE determine if species and/or wear stage had a significant effect on studies (Bunn et al., 2011; Winchester et al., 2014), but tend to dental topographic results. Tooth size was analyzed with dental oversimplify large and complex teeth (Berthaume and Schroer, topographic results as topographic scores can predict diet more 2017). A triangle count of 20,000 was suggested by Berthaume efficiently when tooth size is included (Bunn et al., 2011; and Schroer (2017), but higher triangle counts have been recom- Winchester et al., 2014). Kendall's and Pearson's correlations mended for other dental topographic metrics (e.g., 22,000 and were used to evaluate the strength of the relationship between 55,000; Guy et al., 2013, 2015; Lazzari and Guy, 2014; Thiery et al., shape (DNE, OPCR, RFI, and PCV) and size and wear scores within 2017a). Simplified and full versions of the teeth were imported into each species. Exact p-values were calculated for Pearson's correla- CloudCompare (2017) and oriented into anatomically correct po- tion, but not Kendall's due to ties. Pearson's pairwise correlations sition, using fossils with portions of the mandible preserved as were run between shape and size values to determine if any rela- guides. Specimen specific deviations from the procedure detailed in tionship existed among these metrics. Dental topographic variables this section can be found in the SOM Table S2. were analyzed separately. As wear had a significant effect on some shape and size values, 2.3. Calculating shape and size one-way ANOVAs were run on moderate and lightly worn teeth separately to determine if there was any difference in shape and DNE, RFI, OPCR, and tooth size were calculated using Morpho- size values between species in R and RStudio (R Development Core tester (Winchester, 2016). Two values were reported for DNE, Team, 2015; RStudio Team, 2016). Tukey's honestly significant dif- removing the top 1% (DNE 99%) and 5% (DNE 95%) energy area ference (HSD) tests were run to determine where significant dif- values, as taphonomic processes can cause an unusually high ferences occurred between species. Mann-Whitney U-tests and number of sharp edges at fissures on the occlusal surface. This Student's t-tests were run to determine if there was any difference causes artificial inflations in DNE scores when 1% outlier removal in cropping methods. Although previous studies have shown there was used; 5% outlier removal discarded these artifacts. RFI is a is a phylogenetic signal in tooth shape and size (Winchester et al., function of surface and cross-sectional areas (Boyer, 2008): RFI ¼ ln 2014), it is not possible for us to run phylogenetically corrected (sqrt(SA/CA)). Cross-sectional area is also the measure of tooth size. analyses as there is no secure, agreed, or well-quantified phylogeny OPCR here is not directly comparable to OPCR calculated using 2.5D for these taxa. surfaces with regular grids (Evans et al., 2007; Wilson et al., 2012; Evans, 2013; Winchester, 2016), but is correlated. PCV was calcu- 3. Results lated in CloudCompare using the ‘PCV’ function, with the ’fits a fi ‘ statistical model on the active scalar eld command, which reports Forty-three hominin M2 from eight sites were included in the on an average PCV value (Berthaume, 2016a). Dental topography dental topographic analysis (Table 1; SOM Table S2). Descriptive was performed on surfaces simplified to 10,000 triangles, as is dental topographic statistics can be found in Table 2. Additional typical in dental topographic studies (e.g., Godfrey et al., 2012; descriptive statistics for different triangle counts and cropping Winchester et al., 2014) and 20,000 triangles, as occlusal features methods can be found in the SOM Tables S3 to S5. As in previous were better preserved at 20,000 triangles. It is important to keep studies, significant relationships exist between many shape and triangle count constant, as some dental topographic metrics are size variables (Table 3). Relationships between shape and size sensitive to triangle count (e.g., DNE and OPCR; Bunn et al., 2011; variables for different triangle counts and cropping methods are Evans and Janis, 2014). found in SOM Tables S16 to S18. DNE 95% and DNE 99% are corre- To contextualize the hominin DNE results, they are compared to lated to all other metrics (positively with each other, OPCR and RFI, published DNE results on great apes (Berthaume and Schroer, negatively with PCV), and a negative correlation exists between RFI 2017). As the great ape data were collected with the BCO crop- and PCV. Tooth size is correlated to PCV and RFI. Given the low ping method, we employed both the EEC and BCO and investigated sample of Homo sp. (n ¼ 3), it was excluded from statistical analyses the effect of cropping method on our results. Finally, as great ape but compared to the range of values for the other taxa. data used Laplacian smoothing, which affects DNE results (Spradley et al., 2017), hominin teeth had Laplacian smoothing applied when 3.1. Wear compared to the great ape data. Similar to previous studies (M'Kirera and Ungar, 2003; Ungar 2.4. Tooth wear and M'Kirera, 2003), a two-way ANOVA showed many topo- graphic metrics were significantly affected by occlusal wear and As in previous studies (M'Kirera and Ungar, 2003; Ungar and M'Kirera, 2003), tooth wear was scored using Scott's (1979) Table 1 Hominin sample used in this study. For fossil accession numbers, see SOM. dental scoring technique. However, it was modified, where the entoconid, metaconid, protoconid, hypoconid, and hypoconulid Taxon Lightly worn Moderately worn were each scored from 0 to 10, where a score of 3 indicates cusps Australopithecus africanus 10 7 had significant wear, but no dentin was exposed and cusps retained Paranthropus robustus 78 their relative curvature (Scott, 1979). When additional cusps were Homo naledi 53 Homo sp. 1 2 present, they were not scored. A final wear score was calculated by 18 M.A. Berthaume et al. / Journal of Human Evolution 118 (2018) 14e26

Table 2 Descriptive statistics for more lightly and moderately worn lower second molars.a

Wear DNE 99% DNE 95% RFI

Mean Median SE Mean Median SE Mean Median SE

A. africanus Light (10) 250.212 249.331 7.548 390.297 408.791 11.172 0.458 0.463 0.003 Moderate (7) 110.942 114.988 2.45 166.485 163.979 5.595 0.423 0.439 0.005 P. robustus Light (7) 244.926 252.743 12.314 464.911 466.126 24.868 0.494 0.492 0.003 Moderate (8) 165.653 129.183 13.126 224.91 201.317 13.23 0.451 0.464 0.006 H. naledi Light (5) 244.694 250.378 4.491 547.846 592.637 24.412 0.538 0.536 0.002 Moderate (3) 152.998 155.172 14.023 270.042 277.952 28.776 0.465 0.477 0.014 Homo sp. Light (1) 155.172 155.172 e 277.952 277.952 e 0.477 0.477 e Moderate (2) 120.529 120.529 e 192.5 192.5 e 0.395 0.395 e

OPCR PCV Size

Mean Median SE Mean Median SE Mean Median SE

A. africanus Light (10) 168.388 158.5 4.132 0.58 0.582 0.001 203.107 207.394 2.47 Moderate (7) 123.5 121.125 2.267 0.614 0.606 0.003 187.529 184.391 4.097 P. robustus Light (7) 148.696 142 5.463 0.556 0.552 0.002 205.045 208.778 3.938 Moderate (8) 161.594 155.875 5.617 0.601 0.6 0.004 203.794 194.643 4.708 H. naledi Light (5) 143.625 143.625 1.787 0.513 0.506 0.003 133.227 131.926 1.507 Moderate (3) 148.083 148.5 2.336 0.536 0.542 0.006 138.649 134.145 3.882 Homo sp. Light (1) 148.5 148.5 e 0.542 0.542 e 134.145 134.145 e Moderate (2) 193.625 193.625 e 0.686 0.686 e 153.006 153.006 e

a Cropping method ¼ EEC. Triangle count ¼ 20,000.

Table 3 Coefficient of correlation (R), followed by p-values in parentheses for Pearson's pairwise comparisons between form variables. Significant correlations (p < 0.05) are in bold.a

DNE 99% DNE 95% RFI OPCR PCV

DNE 95% 0.819 (0) RFI 0.654 (0) 0.504 (0.001) OPCR 0.355 (0.025) 0.465 (0.002) 0.102 (0.532) PCV ¡0.702 (0) ¡0.527 (0) ¡0.8 (0) 0.061 (0.707) Tooth size 0.215 (0.182) 0.125 (0.444) ¡0.387 (0.014) 0.027 (0.871) 0.468 (0.002)

a Cropping method ¼ EEC. Triangle count ¼ 20,000. p-values of 0 are less than 0.0005.

taxon, but not the interaction variable between wear and taxon intersection of the cusps. Differences in DNE, OPCR, and PCV due to (Table 4). Additional two-way ANOVAs for different triangle counts wear are easily visible for each taxon (Fig. 2; note that RFI is a ratio and cropping methods are found in SOM Tables S6 to S8. Taxon is and cannot be visualized). Kendall's correlations between wear and important for DNE 99%, but not DNE 95%dthis difference is due to shape and size metrics within each taxon revealed significant cor- the top 5% of the ‘curviest’ parts of the surface being disregarded in relations between tooth wear and a) DNE 99% and DNE 95% in all DNE 95% compared to the top 1% in DNE 99%. The drastic change in taxa (p < 0.001e0.034); b) PCV in P. robustus and H. naledi results is due to a large number of highly curvy singularities on the (p < 0.001); c) RFI in P. robustus (p < 0.001); and d) OPCR in A. surface of the tooth, usually located at the fissures that form at the africanus (p ¼ 0.044; Table 5). Wear was never significantly corre- lated to tooth size (p ¼ 0.111e0.618), despite the presence of fi Table 4 interproximal wear, which can signi cantly affect tooth size (Wood Results of two-way ANOVA investigating the effect of wear stage and taxon on and Abbott, 1983). This could be because we did not include heavily dental topographic results. Significant p-values (p < 0.05) are in bold.a worn teeth in our analysis. Kendall's correlations for other triangle

Factor Degrees of freedom F p counts and cropping methods are found in SOM Tables S9 to S11. Pearson's correlations revealed nearly identical results (SOM DNE 99% Taxon 2 6.68 0.004 Wear stage 1 73.838 0 Tables S12 to S15), and, as such, are not reported here. We there- Taxon wear stage 2 1.051 0.361 fore analyzed lightly worn (Scott score < 3) and moderately worn DNE 95% Taxon 2 0.304 0.74 (Scott score 3þ) teeth separately. Wear stage 1 45.935 0 Taxon wear stage 2 0.221 0.803 RFI Taxon 2 19.293 0 Wear stage 1 41.341 0 3.2. Cropping method Taxon wear stage 2 2.97 0.065 OPCR Taxon 2 0.225 0.8 Wear stage 1 1.019 0.32 Both Mann-Whitney U-tests and Student's t-tests yielded Taxon wear stage 2 2.161 0.131 identical results: regardless of triangle count or shape/size metric, PCV Taxon 2 56.701 0 cropping method caused a statistically significant difference in Wear stage 1 71.158 0 dental topographic values (p < 0.001e0.006; Table 6 and SOM Taxon wear stage 2 3.26 0.051 Tooth size Taxon 2 18.298 0 Table S26). Since EEC provides information about relative crown Wear stage 1 0.09 0.766 height, EEC results were used to compare the hominins to each Taxon wear stage 2 1.054 0.36 other; however, as the ape teeth were analyzed using BCO (due to a Cropping method ¼ EEC. Triangle count ¼ 20,000. p-values of 0 are less than differences in data acquisition which prevent EEC from being used), 0.0005. BCO was used to compare the hominin and ape data. M.A. Berthaume et al. / Journal of Human Evolution 118 (2018) 14e26 19

Figure 2. Lightly worn (gray background) and moderately worn M2 for Australopithecus africanus (STW 560E and 109), Paranthropus robustus (DNH 60c, SK 858), Homo naledi (U.W. 101e307 and U.W. 101e1261), and South African Homo sp. (Cave of Hearths and STW 80) with dental topographic scores approaching the average for each species. Dark blue triangles along the cervical margin and at the intersections of the cusps in the DNE 99% pictures represent triangles discarded using 1% outlier removal (energy area). Note that STW 80 is mirrored to make it comparable to the other teeth in the 3D views. Teeth are not to scale. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

3.3. Taxonomic differences between A. africanus and P. robustus in moderately worn teeth (SOM Tables S19 to S22). In lightly worn teeth, a Tukey HSD test One-way ANOVAs revealed taxonomic differences in RFI, PCV, revealed taxonomic differences in RFI and PCV, with H. naledi and tooth size in lightly worn teeth (p < 0.001). The small sample having the highest RFI, followed by P. robustus, then A. africanus size of moderately worn H. naledi teeth (n ¼ 3; Table 1) prevented (Table 7). The opposite trend is found with PCV, indicating H. naledi their inclusion in these statistical analyses. No differences existed had the most wear resistant teeth, followed by P. robustus, then A. 20 M.A. Berthaume et al. / Journal of Human Evolution 118 (2018) 14e26

Table 5 Table 7 Kendall's correlations between wear and form metrics, broken up by species. Sig- Tukey HSD test results from one-way ANOVAs. Significant relationships (p < 0.05) nificant p-values (p < 0.05) are in bold.a are in bold.a

Species Tau t p Comparison Lightly worn Moderately worn

DNE 99% A. africanus 0.638 3.302 0.001 Difference p Difference p P. robustus 0.73 3.857 0 DNE 99% H. naledi-A. africanus 157.549 0.115 ee H. naledi 0.645 2.125 0.034 H. naledi-P. robustus 82.935 0.563 ee DNE 95% A. africanus 0.692 3.578 0 P. robustus-A. africanus 74.614 0.52 58.425 0.192 P. robustus 0.575 3.04 0.002 DNE 95% H. naledi-A. africanus 5.519 0.989 ee H. naledi 0.806 2.657 0.008 H. naledi-P. robustus 0.232 1 ee RFI A. africanus 0.266 1.376 0.169 P. robustus-A. africanus 5.286 0.988 54.711 0.198 P. robustus 0.73 3.857 0 RFI H. naledi-A. africanus 0.08 0 ee H. naledi 0.564 1.86 0.063 H. naledi-P. robustus 0.043 0.027 ee OPCR A. africanus 0.39 2.018 0.044 P. robustus-A. africanus 0.036 0.028 0.027 0.21 P. robustus 0.026 0.136 0.892 OPCR H. naledi-A. africanus 24.763 0.434 ee H. naledi 0.081 0.266 0.79 H. naledi-P. robustus 5.071 0.968 ee PCV A. africanus 0.692 3.578 0 P. robustus-A. africanus 19.691 0.518 38.094 0.054 P. robustus 0.678 3.585 0 PCV H. naledi-A. africanus 0.067 0 ee H. naledi 0.322 1.063 0.288 H. naledi-P. robustus 0.043 0 ee Tooth size A. africanus 0.195 1.009 0.313 P. robustus-A. africanus 0.024 0.013 0.012 0.411 P. robustus 0.094 0.499 0.618 Tooth size H. naledi-A. africanus 69.88 0 ee H. naledi 0.483 1.594 0.111 H. naledi-P. robustus 71.817 0 ee a Cropping method ¼ EEC. Triangle count ¼ 20,000. p-values of 0 are less than P. robustus-A. africanus 1.938 0.984 16.265 0.37 0.0005. a p-values of 0 are less than 0.0005.

Table 6 moderately worn sample. This discrepancy is likely due to a small Mann-Whitney U-test results, testing the effect of cropping method (EEC vs. BCO). Regardless of wear stage, triangle count, or form metric, results are always sensitive sample in Homo sp. (Fig. 3; SOM Table S2). Compared to the great to cropping method. Significant p-values (p < 0.05) are in bold.a apes, all hominins had curvier, sharper teeth (Fig. 4, Table 8). To further contextualize the results, they were compared to Wear stage Triangle count Variable U-value p published great ape data (Berthaume and Schroer, 2017; Fig. 4). For Lightly worn 20,000 DNE 99% 4010 0.006 the sake of comparison, DNE 99% was performed on teeth with the DNE 95% 4084 0.002 RFI 0 0 basin cut off (BCO) cropping method with Laplacian smoothing OPCR 4954 0 (Spradley et al., 2017). One-way ANOVA and Tukey HSD tests reveal PCV 5922 0 that P. robustus and H. naledi have curvier teeth than all great apes Size 2128 0 (p < 0.0005e0.02; Table 8). A. africanus has curvier teeth than Pan, 10,000 DNE 99% 4010 0.006 DNE 95% 4084 0.002 but no differences exist between A. africanus and Gorilla or Pongo. RFI 0 0 Processing the teeth in this manner also caused a difference in DNE OPCR 4954 0 to develop between A. africanus and H. naledi (p < 0.001), indicating PCV 5922 0 significant differences in DNE 99%. The M2 of the Cave of Hearths Size 2128 0 Homo mandible falls within the DNE range of all apes except for Pan Moderately worn 20,000 DNE 99% 4010 0.006 DNE 95% 4084 0.002 troglodytes troglodytes. RFI 0 0 OPCR 4954 0 PCV 5922 0 4. Discussion Size 2128 0 10,000 DNE 99% 4010 0.006 It has been observed that there is very low variation in tooth DNE 95% 4084 0.002 RFI 0 0 shape in H. naledi when compared to other hominins (Skinner et al., OPCR 4954 0 2016; Delezene et al., 2017). For lightly worn teeth in this study, PCV 5922 0 H. naledi has the lowest level of coefficient of variation for five of Size 2128 0 the six shape and size variables (Homo sp. was excluded because of a p-values of 0 are less than 0.0005. sample size; Table 9). Overall, it appears that there is less variation in tooth shape in H. naledi than in A. africanus or P. robustus, which could be due to a) low variation within the species, b) the H. naledi africanus. Significant differences exist between H. naledi and sample in this study being from a single chamber (i.e., the Dinaledi P. robustus/A. africanus in tooth size, but no difference in tooth size chamber), whereas both A. africanus and P. robustus are represented existed between A. africanus and P. robustus. Boxplots of shape and from several sites spanning a larger temporal and geographical size values are shown in Figure 3 for lightly worn teeth. Descriptive range, or c) chance sampling and low sample sizes. statistics and additional boxplots, ANOVAs, and Tukey HSD tests for As in previous studies (e.g., M'Kirera and Ungar, 2003; Ungar moderately worn teeth, and different cropping methods and tri- and M'Kirera, 2003; King et al., 2005; Glowacka et al., 2016; angle counts, which produced the same pattern of results, can be Pampush et al., 2016), tooth wear played a significant role in found in SOM Tables S19 To S25. some of the dental topographic metrics. As expected, wear caused Although the small sample size for Homo sp. prohibits statistical DNE 99%, DNE 95% and RFI to decrease, indicating the teeth were analyses, it appears that H. naledi differs from Homo sp. in the same becoming duller and lower crowned (Figs. 2 and 3). Wear caused direction that it differs from A. africanus and P. robustus (Figs. 2 and PCV to increase, indicating teeth became less wear resistant as they 3). Additionally, H. naledi may differ from Homo sp. in DNE 99% and became more worn. OPCR was uncorrelated to tooth wear, which DNE 95%. Compared to Homo sp., H. naledi has relatively larger initially seemed counterintuitive as teeth lose ‘tools’ (e.g., crenu- teeth when in the lightly worn sample, but smaller teeth in the lations) as they wear. However, in the initial stages of wear, the M.A. Berthaume et al. / Journal of Human Evolution 118 (2018) 14e26 21

Figure 3. Dental topographic and tooth size results, per species, for lightly worn teeth (average Scott score < 3). Triangle count ¼ 20,000. Cropping method ¼ EEC. cusps and crests are all still essentially salient, which may be why P. robustus, A. africanus,andH. naledi suggests that the teeth of OPCR was not related to wear. It may only be in later stages of wear, H. naledi arenomoreorlessefficient at chewing foods with struc- when crests and cusps are obliterated and large dentin pools begin tural fibers than are those of A. africanus and P. robustus. In other to form, that OPCR is significantly correlated to wear in hominins. words, the differences in dental topography among the hominin Although changes in tooth size occur due to interproximal wear samples may not reflect a shift towards lower quality foods such as (Wood and Abbott, 1983), intraspecific variation plays a larger role grasses or sedges in H. naledi. Instead, the increases in dental in variation in M2 size in this study. longevity could be due to consuming foods with similar mechanical Homo naledi displays a unique combination of dental topographic properties but different phytolith loads, or increased dust/grit con- traits relative to other South African hominins, suggesting that this sumption (Lucas et al., 2013; Kaiser et al., 2015; Madden, 2015; Xia taxon could have occupied its own ecological niche. Within lightly et al., 2015). The absolutely smaller molars in H. naledi relative to worn teeth, H. naledi had the highest crowned (RFI) and most wear A. africanus and P. robustus suggest that the former was not resistant (PCV) molars, indicating an adaptation for tooth longevity. consuming more mechanically challenging foods and further sup- The lack of differences in tooth sharpness (DNE) and the number of port the conclusion that H. naledi was not consuming foods that ‘tools’ on the occlusal surface (dental complexity, OPCR) of require bulk processing, such as grasses or sedges. 22 M.A. Berthaume et al. / Journal of Human Evolution 118 (2018) 14e26

Table 8 Great ape DNE (BCO, 20,000) compared to the hominins.a Differences between mean DNE scores are followed by p-values. Significant p-values (p < 0.05) are in bold.b

Pa. t. troglodytes Pa. paniscus Pa. t. schweinfurthii Po. pygmaneus G. g. gorilla G. b. beringei G. b. graueri A. africanus P. robustus

Pa. paniscus 99.107 (0.905) Pa. t. schweinfurthii 86.446 (0.965) 12.661 (1) Po. pygmaneus 188.431 (0.141) 89.323 (0.939) 101.985 (0.892) G. g. gorilla 110.255 (0.857) 11.148 (1) 23.809 (1) 78.176 (0.979) G. b. beringei 132.533 (0.637) 33.425 (1) 46.087 (1) 55.898 (0.998) 22.278 (1) G. b. graueri 233.652 (0.041) 134.545 (0.657) 147.206 (0.575) 45.221 (1) 123.397 (0.787) 101.119 (0.91) A. africanus 306.926 (0) 207.819 (0.037) 220.48 (0.03) 118.495 (0.614) 196.671 (0.081) 174.393 (0.146) 73.274 (0.978) P. robustus 500.758 (0) 401.651 (0) 414.312 (0) 312.327 (0.001) 390.503 (0) 368.225 (0) 267.106 (0.02) 193.832 (0.123) H. naledi 735.098 (0) 635.99 (0) 648.651 (0) 546.667 (0) 624.843 (0) 602.565 (0) 501.446 (0) 428.171 (0) 234.339 (0.165)

a Great ape data are from Berthaume and Schroer (2017). b p-values of 0 are less than 0.0005.

Figure 4. Ape vs. hominin DNE using published ape data (20,000 triangles, DNE 99%, BCO, lightly worn, Laplacian smoothing ¼ 2; Berthaume and Schroer, 2017). As in a previous study (Spradley et al., 2017), Laplacian smoothing caused DNE to decrease from 3.62 to 23.67% for all teeth (except SKX 4446, which has a 40% increase), but was necessary to make the hominin data comparable to the ape data. Hominin data was recalculated with the BCO to make it comparable to the great ape data. All comparisons without the apes were done using the entire enamel cap (EEC) without Laplacian smoothing. Abbreviations: Ptt ¼ Pan troglodytes troglodytes; Ppa ¼ Pan paniscus; Pts ¼ Pan troglodytes schweinfurthii; Ppy ¼ Pongo pygmaeus; Ggg ¼ Gorilla gorilla gorilla; Gbb ¼ Gorilla beringei beringei; Gbg ¼ Gorilla beringei graueri;Aa¼ Australopithecus africanus; Pr ¼ Paranthropus robustus; Hn ¼ Homo naledi; Hsp ¼ Homo sp.

There are two probable adaptive scenarios for an increase in organs, which, if unwashed, would transfer large amounts of grit to dental longevity in H. naledi. The first is a dietary shift towards the oral cavity. The second is an environmental (climatic) shift to- foods with a higher abrasive load, such as phytoliths, dust, or grit. A wards increased aridity led to an incidental increase in dust and/or probable candidate for such foods would be underground storage grit consumption, affecting all food sources. Among A. africanus, M.A. Berthaume et al. / Journal of Human Evolution 118 (2018) 14e26 23

Table 9 Previous hominin dental topographic studies (Ungar, 2004, Coefficients of variation (standard deviation/mean) for shape and size variables 2007) have reported that Homo sp. had molar cusps with steeper (EEC, 20,000, lightly worn teeth). slopes and higher relief than Australopithecus afarensis, and that DNE 99% DNE 95% RFI OPCR PCV Size A. africanus had molar cusps with steeper slopes compared to Australopithecus Unworn (10) 0.286 0.302 0.070 0.245 0.026 0.122 P. robustus. However, Ungar (2004, 2007) did not calculate RFI for africanus Worn (7) 0.235 0.155 0.083 0.128 0.029 0.153 the South African sample. The reported difference in RFI in this Paranthropus Unworn (7) 0.374 0.352 0.045 0.257 0.025 0.134 study show A. africanus to have lower relief than P. robustus (Fig. 3, robustus Worn (8) 0.471 0.634 0.098 0.278 0.058 0.185 Table 7), which is the opposite of what is expected given the cor- Homo naledi Unworn (5) 0.223 0.092 0.020 0.062 0.033 0.057 Worn (3) 0.320 0.275 0.090 0.047 0.032 0.084 relation between slope and RFI in the east African hominins and great apes reported in Ungar (2004, 2007), although this could be due to differences in cropping methods (EEC vs. BCO). To investi- gate if this was the case, we used the same cropping method as P. robustus, and H. naledi, temporal increases in relative crown Ungar (2004, 2007) to make our results comparable. Using the BCO height (RFI) and wear resistance (PCV) are coincident with an cropping method produced the same results as using the EEC: the increasingly dry and arid environment (Vrba, 1975, 1985; Lee-Thorp molar cusps of A. africanus still had lower relief than P. robustus, et al., 2007). Therefore, it is possible that the foods being consumed although the difference was no longer statistically significant by H. naledi had more inorganic abrasives on them, which required (p ¼ 0.122e0.133; SOM Figs. S1 to S7 and Tables S3 to S5). This more wear-resistant molars. A recent study (Towle et al., 2017) suggests that there is some discordance among the hominin dental reported an extremely high level of dental chipping in H. naledi, topographic results, where it may be possible for some hominins to suggesting the increase in dental longevity could be an adaptation have cusps with steeper slopes and higher relief, and others to have to offset high levels of wear due to accidental grit consumption. It is steeper slopes and lower reliefda discordance that must be not possible from our data to discern whether this is because of a remedied to provide better dietary reconstructions through dental dietary (e.g., underground storage organs, USOs) or an environ- topographic analyses using these methods. mental shift. Data from stable carbon isotope and dental microwear Ungar (2004, 2007) reported on differences in hominin cusp analyses for H. naledi (e.g., Henry et al., 2012) will shed light on this slope that mirrored those found in chimpanzees and gorillas. Based issue. on similarities in primary diet in P. troglodytes and Gorilla gorilla, The great apes were found to have duller, less curvy teeth than but differences in fallback foods, Ungar (2004, 2007) concluded hominins in some analyses (Fig. 4). This may seem odd that, given that differences in tooth shape reflected differences in fallback their generally taller cusps generate relatively longer shearing foods, and that the hominins, Homo sp. and A. africanus, fell back on crests that would, presumably, increase tooth sharpness. However, ‘tougher’ foods than A. afarensis and P. robustus, respectively. Since it appears that the extremely crenulated surfaces of some hominin these pioneering studies, research has shown that dental topog- teeth (i.e., A. africanus and P. robustus) may be making their occlusal raphy frequently reflects primary diet in primates (e.g., Winchester surfaces, overall, sharper: but this cannot be the case for H. naledi, et al., 2014; Berthaume and Schroer, 2017), so differences in tooth which lacks crenulations (L.K.D., pers. obs.). The relatively higher shape may reflect differences in preferred, not fallback, foods. It DNE values in H. naledi, A. africanus, and P. robustus imply their diets appears that, from a topographic perspective, the relationship be- required higher shear forces, for eating substances such as plant tween tooth form and preferred vs. fallback food is not straight- fiber and/or muscle fiber, compared to the great apes. Sharper teeth forward. A recent study on great apes additionally showed that are more efficient at producing high shear forces during mastica- comparing allopatric hominoids must be done carefully, as char- tion, which is advantageous for processing foods high in structural acter displacement has occurred in great ape tooth shape due to fibers; this is the reason primates that consume more plant fiber indirect competition over dietary resources (Berthaume and have higher DNE values (Godfrey et al., 2012; Winchester et al., Schroer, 2017), although, fortunately, the signature for relative fi- 2014; Berthaume and Schroer, 2017). Foods high in structural fi- ber content appears to be unaffected by this evolutionary phe- ber can be low (e.g., grasses, sedges, bark, and leaves) or high (e.g., nomenon. The fact that H. naledi was temporally separated, and USOs, muscle fascicles and fibers) quality.2 Therefore, from a therefore allochronic from the other hominins in our sample (Dirks fracture mechanics perspective, the higher DNE in A. africanus, et al., 2015), hinders an easy interpretation of the results of this P. robustus, and H. naledi could be an adaptation towards consuming study. Without more associated faunal material, or other informa- a large range of resources requiring shear forces to process. Relative tion on the paleoenvironment of H. naledi (see Dirks et al., 2015), it to the great apes and the other hominins, the apparent reversion in is currently impossible to determine if the competitive environ- DNE with Homo sp. could have occurred due to a dietary shift to- ment in South Africa was similar from the early to the late Middle wards foods requiring lower shear forces, because the introduction Pleistocene, the time interval in which A. africanus, P. robustus, of cooking and/or food processing relaxed the selective forces Homo sp., and H. naledi existed. However, from a perspective of the acting on tooth sharpness (Wrangham, 2009; Zink et al., 2014), or functional morphology of the molars, H. naledi seems unlikely to because their diet did not require high shear forces to process. It is have had an Australopithecus-like pattern of resource exploitation, unlikely that differences in DNE are environmentally driven, as despite sharing similarities in brain size, body size, and hand and differences in DNE have not been shown to be correlated with grit/ shoulder morphology (Berger et al., 2017). dust consumption and/or tooth longevity. It could be argued that a drawback of this study comes from the potential decoupling between morphology and diet. Dietary sig- natures drawn from morphology do not always match dietary

2 Foods high in structural fiber have traditionally been classified as ‘tough,’ but it signatures from other methods, such as stable carbon isotope or is recommended that this term not be used, as toughness has more than one dental microwear analyses. This was thought to be the case with definition in materials science (Berthaume, 2016b). Toughness, as used by Lucas Paranthropus boisei, which has large teeth and a powerfully-built (2004), is energy release rate. Objects with high energy release rates resist shear skull coupled with large chewing muscles, leading many to and tensile fracture with variable levels of efficiency. In plants, energy release rate expect that it consumed hard foods, such as nuts or seeds (Jolly, and fiber content are correlated (Lucas et al., 2000; Westbrook et al., 2011), and plants with high energy release rates are most efficiently processed with shear 1970; Rak, 1983; Demes and Creel, 1988; Dzialo et al., 2013; forces. Smith et al., 2015). However, more recent isotope and microwear 24 M.A. Berthaume et al. / Journal of Human Evolution 118 (2018) 14e26 work has suggested it ate larger amounts of low quality, mechan- Temming, Patrick Schoenfeld, Collin Moore, Tracy Kivell and Adam ically challenging foods, such as grasses, sedges, or underground Sylvester. Finally, we thank Myra Laird, David Katz, John Hawks, storage organs (Ungar et al., 2008; Cerling et al., 2011; Grine et al., and Lee Berger for useful comments and discussions on the 2012). This and other discrepancies between morphology and iso- manuscript. topes/microwear have led some researchers to question whether morphology can be used to predict diet (Strait et al., 2009, 2012, Supplementary Online Material 2013; Grine et al., 2010; Daegling et al., 2013). This debate was further fueled by observed discrepancies between morphology and Supplementary online material related to this article can be diet in extant taxa (e.g., King et al., 2005). But this need not be the found at https://doi.org/10.1016/j.jhevol.2018.02.006. case, as isotope/microwear analyses can be used in conjunction with morphological analyses to produce new hypotheses about the References diets of extinct taxa (Dominy et al., 2008; Macho, 2014). Allen, K.L., Cooke, S.B., Gonzales, L.A., Kay, R.F., 2015. Dietary inference from upper 5. Conclusions and lower molar morphology in platyrrhine primates. PLoS One 10, e0118732. Anton, S.C., Potts, R., Aiello, L.C., 2014. Evolution of early Homo: an integrated biological perspective. Science 345, 1236828. Overall, H. naledi has smaller, higher-crowned and wear resis- Berger, L.R., Hawks, J., de Ruiter, D.J., Churchill, S.E., Schmid, P., Delezene, L.K., tant teeth than A. africanus and P. robustus. Thus, despite similarities Kivell, T.L., Garvin, H.M., Williams, S.A., DeSilva, J.M., Skinner, M.M., in brain size, body size, and hand and shoulder anatomy suggesting Musiba, C.M., Cameron, N., Holliday, T.W., Harcourt-Smith, W., Ackermann, R.R., Bastir, M., Bogin, B., Bolter, D., Brophy, J., Cofran, Z.D., Congdon, K.A., Deane, A.S., ecological constraints and environmental exploitation similar to Dembo, M., Drapeau, M., Elliott, M.C., Feuerriegel, E.M., Garcia-Martinez, D., Australopithecus (Kivell et al., 2015; Feuerriegel et al., 2017; Garvin Green, D.J., Gurtov, A., Irish, J.D., Kruger, A., Laird, M.F., Marchi, D., Meyer, M.R., et al., 2017), the results of this study suggest that H. naledi teeth are Nalla, S., Negash, E.W., Orr, C.M., Radovcic, D., Schroeder, L., Scott, J.E., Throckmorton, Z., Tocheri, M.W., VanSickle, C., Walker, C.S., Wei, P., Zipfel, B., distinct in functional anatomy from those of Australopithecus and 2015. 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Food mechanical properties and dietary ecology. American Homo sp., both the older material from Swartkrans and Sterkfontein Journal of Physical Anthropology 159, 79e104. and the younger specimen from the Cave of Hearths. These differ- Berthaume, M.A., Schroer, K., 2017. Extant ape dental topography and its implica- ences in dental morphology, in conjunction with differences in DNE tions for reconstructing the emergence of early Homo. Journal of Human Evo- lution 112, 15e29. 99% and DNE 95%, suggest the potential for ecological differentia- Berthaume, M., Grosse, I.R., Patel, N.D., Strait, D.S., Wood, S., Richmond, B.G., 2010. tion between H. naledi and other South African Homo as well. The The effect of early hominin occlusal morphology on the fracturing of hard food results of this study are thus inconsistent with the simple notion items. Anatomical Record 293, 594e606. Boyer, D.M., 2008. Relief index of second mandibular molars is a correlate of diet that H. naledi represents a hominin in the Middle Pleistocene with among prosimian primates and other euarchontan mammals. Journal of Human an Australopithecus-like ecology, or that African Middle Pleistocene Evolution 55, 1118e1137. Homo were adaptively and ecologically uniform. Whether differ- Boyer, D.M., Costeur, L., Lipman, Y., 2012. Earliest record of Platychoerops (Primates, fl Plesiadapidae), a new species from Mouras Quarry, Mont de Berru, France. ences in dental shape and size re ect adaptations to dietary or American Journal of Physical Anthropology 149, 329e346. environmental (e.g., grit loads) factors, we cannot say now. How- Bunn, J.M., Boyer, D.M., Lipman, Y., St Clair, E.M., Jernvall, J., Daubechies, I., 2011. ever, these differences do provide context for interpreting future Comparing Dirichlet normal surface energy of tooth crowns, a new technique of fi microwear and isotopic studies of the taxa (e.g., Henry et al., 2012) molar shape quanti cation for dietary inference, with previous methods in isolation and in combination. American Journal of Physical Anthropology 145, and highlight the need for paleoenvironmental reconstructions for 247e261. the Rising Star hominin sites. Cerling, T.E., Mbua, E., Kirera, F.M., Manthi, F.K., Grine, F.E., Leakey, M.G., Sponheimer, M., Uno, K.T., 2011. Diet of Paranthropus boisei in the early Pleis- tocene of East Africa. Proceedings of the National Academy of Sciences of the Acknowledgements United States of America 108, 9337e9341. CloudCompare (version 2.6.2) [GPL software], 2017. Retrieved from: http://www. The authors thank The National Geographic Society, The Na- cloudcompare.org/. fi Daegling, D.J., Judex, S., Ozcivici, E., Ravosa, M.J., Taylor, A.B., Grine, F.E., Teaford, M.F., tional Research Foundation, the Paleontological Scienti c Trust, and Ungar, P.S., 2013. Viewpoints: feeding mechanics, diet, and dietary adaptations the Lyda Hill Foundation for funding the excavation and analysis of in early hominins. American Journal of Physical Anthropology 151, 356e371. the Rising Star fossils. This research was supported by the Delezene, L.K., Irish, J.D., Skinner, M.M., Brophy, J.K., Hawks, J., Berger, L.R., 2017. Metric variation in Homo naledi molars. American Journal of Physical Anthro- Department of Human Evolution and the Max Planck Weizmann pology 162, 160. Center for Integrative Archaeology and Anthropology, both parts of Demes, B., Creel, N., 1988. Bite force, diet, and cranial morphology of fossil homi- the Max Planck Institute for Evolutionary Anthropology, with funds nids. Journal of Human Evolution 17, 657e670. Dennis, J.C., Ungar, P.S., Teaford, M.F., Glander, K.E., 2004. Dental topography and from the Max Planck Society (M.B. and K.K.). Financial support for molar wear in Alouatta palliata from Costa Rica. American Journal of Physical L.K.D. was provided by a Connor Family Faculty Fellowship and the Anthropology 125, 152e161. Office of Research and Development at the University of Arkansas. Dirks, P.H., Berger, L.R., Roberts, E.M., Kramers, J.D., Hawks, J., Randolph- For logistical support and access to the fossils of H. naledi, we thank Quinney, P.S., Elliott, M., Musiba, C.M., Churchill, S.E., de Ruiter, D.J., Schmid, P., Backwell, L.R., Belyanin, G.A., Boshoff, P., Hunter, K.L., Feuerriegel, E.M., Lee Berger, John Hawks, and the staff at the Evolutionary Studies Gurtov, A., Harrison, J., du, G., Hunter, R., Kruger, A., Morris, H., Makhubela, T.V., Institute. For access to the comparative sample and scans of the Peixotto, B., Tucker, S., 2015. Geological and taphonomic context for the new specimens, we thank Stephany Potze (Ditsong National Museum of hominin species Homo naledi from the Dinaledi Chamber, South Africa. eLife 4, e09561. Natural History), Bernard Zipfel and Sifelani Jura (University of Dirks, P.H., Roberts, E.M., Hilbert-Wolf, H., Kramers, J.D., Hawks, J., Dosseto, A., Witwatersrand), and Jean-Jacques Hublin (Max Planck Institute for Duval, M., Elliott, M., Evans, M., Grün, R., Hellstrom, J., Herries, A.I., Joannes- Evolutionary Anthropology), as well as Colin Menter and Frances Boyau, R., Makhubela, T.V., Placzek, C.J., Robbins, J., Spandler, C., Wiersma, J., Woodhead, J., Berger, L.R., Roberts, R., VanSickle, C., Walker, C., Campbell, T., Thackeray. For assistance with scanning of this sample, we thank Kuhn, B., Kruger, A., Tucker, S., Hlope, A., Hunter, N., Morris, R., Peixotto, H., Kudakwashe Jakata, Matthew Skinner, Frances Thackeray, Heiko Ramalepa, B., van Rooyen, M., Tsikoane, D., Dirks, P., Berger, L., Negash, E., Orr, C., M.A. Berthaume et al. / Journal of Human Evolution 118 (2018) 14e26 25

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