Danielle F. Royer, 1 * Charles A. Lockwood, 2 Jeremiah E. Scott, 3 and Frederick E. Grine 4,5 NY AZ

Transcription

1 AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 140: (2009) Size Variation in Early Human Mandibles and Molars from Klasies River, South Africa: Comparison with Other Middle and Late Pleistocene Assemblages and with Modern Humans Danielle F. Royer, 1 * Charles A. Lockwood, 2 Jeremiah E. Scott, 3 and Frederick E. Grine 4,5 1 Interdepartmental Doctoral Program in Anthropological Sciences, Stony Brook University, Stony Brook, NY Department of Anthropology, University College London, London, WC1E 6BT, UK 3 School of Human Evolution and Social Change, Institute of Human Origins, Arizona State University, Tempe, AZ Department of Anthropology, Stony Brook University, Stony Brook, NY Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY KEY WORDS heidelbergensis sexual dimorphism; early Homo sapiens; Homo neanderthalensis; Homo ABSTRACT Previous studies of the Middle Stone Age human remains from Klasies River have concluded that they exhibited more sexual dimorphism than extant populations, but these claims have not been assessed statistically. We evaluate these claims by comparing size variation in the best-represented elements at the site, namely the mandibular corpora and M 2 s, to that in samples from three recent human populations using resampling methods. We also examine size variation in these same elements from seven additional middle and late Pleistocene sites: Skhūl, Dolní Věstonice, Sima de los Huesos, Arago, Krapina, Shanidar, and Vindija. Our results demonstrate that size variation in the Klasies assemblage was greater than in recent humans, consistent with arguments that the Klasies people were more dimorphic than living humans. Variation in the Skhūl, Dolní Věstonice, and Sima de los Huesos mandibular samples is also higher than in the recent human samples, indicating that the Klasies sample was not unusual among middle and late Pleistocene hominins. In contrast, the Neandertal samples (Krapina, Shanidar, and Vindija) do not evince relatively high mandibular and molar variation, which may indicate that the level of dimorphism in Neandertals was similar to that observed in extant humans. These results suggest that the reduced levels of dimorphism in Neandertals and living humans may have developed independently, though larger fossil samples are needed to test this hypothesis. Am J Phys Anthropol 140: , VC 2009 Wiley-Liss, Inc. Various studies have proposed that Pleistocene humans, including representatives of early Homo sapiens, H. neanderthalensis, and H. heidelbergensis, were substantially more dimorphic than living humans (e.g., de Lumley and de Lumley, 1973; Brace and Ryan, 1980; Frayer, 1980; Smith, 1980; Wolpoff, 1980; Frayer and Wolpoff, 1985; Bermúdez de Castro et al., 2001; Rosas et al., 2002). In particular, fossils from the Middle Stone Age (MSA) site of Klasies River, South Africa, have been argued to exhibit a higher degree of sexual dimorphism than living humans (Rightmire and Deacon, 1991; Lam et al., 1996). This suggests that levels of dimorphism have decreased fairly recently in our species. Alternatively, work on size variation in the cranial capacity and various postcranial and dental elements of the Sima de los Huesos fossil assemblage (Arsuaga et al., 1997a; Lorenzo et al., 1998; Bermúdez de Castro et al., 2001) and analyses of Neandertal limb bones (Trinkaus, 1980) suggest that these hominins exhibited levels of sexual dimorphism that are indistinguishable from those displayed by modern people. Thus, dimorphism may not have been uniformly higher in Pleistocene hominins than in recent humans. The nature and timing of changes in sexual dimorphism in the Pleistocene remain unclear. In part, this is because of the difficulty of comparing studies that use different methods to estimate dimorphism in fossils, many of which have relied on size as the primary criterion by which to determine sex. Moreover, temporally and geographically mixed samples may introduce size variation from sources other than Additional Supporting Information may be found in the online version of this article. Sadly, Charlie Lockwood passed away prior to the completion of this manuscript. We are confident that he would have been satisfied with our final revisions, and we dedicate this paper to his memory. Grant sponsors: Social Sciences and Humanities Research Council of Canada Doctoral Fellowship (DFR), Leakey Foundation (FEG). *Correspondence to: Danielle F. Royer, Department of Anthropology, Stony Brook University, SBS Building, Room S-501, Stony Brook, NY , USA. droyer@ic.sunysb.edu Received 1 January 2009; accepted 20 February 2009 DOI /ajpa Published online 20 April 2009 in Wiley InterScience ( VC 2009 WILEY-LISS, INC.

2 SIZE VARIATION IN PLEISTOCENE HUMANS 313 sexual dimorphism. Finally, the interpretation of changes in sexual dimorphism in the Pleistocene is further complicated by the differential expression of dimorphism throughout the skeleton (Wood, 1976, 1985; Oxnard, 1987; O Higgins et al., 1990; Lockwood, 1999; Plavcan, 2001, 2002), which makes it nearly impossible to compare fossil samples that preserve different skeletal elements. We use resampling methods to measure size variation and infer the degree of sexual dimorphism in fossil assemblages from eight middle and late Pleistocene sites, thereby applying a uniform statistical method while obviating the need for a priori sex determination. By focusing on temporally and geographically constrained samples of mandibles and molars, which tend to preserve more frequently as fossils than other parts of the skeleton, we are able to directly compare size variation in the same elements across different paleopopulations, while limiting the influence of time and space on sample variation. Klasies River provides the largest single-site assemblage of purported early H. sapiens fossils from sub- Saharan Africa (Singer and Wymer, 1982; Rightmire and Deacon, 1991; Grine et al., 1998; Rightmire et al., 2006). The Klasies River main site preserves two distinct stratigraphic horizons. The lower LBS member is attributed to oxygen isotope stage 5e, with a depositional age of 120 ka, while the overlying SAS member was deposited between 100 and 80 ka (Deacon and Geleijnse, 1988) but may be as young as 63 ka (Millard, 2008). The bulk of the human fossils derive from the younger SAS horizon. The best-represented element in this horizon is the mandibular corpus (n 5 4). Specimen KRM derives from the MSA I deposits of cave IB (Layer 10 of Singer and Wymer, 1982). The others are from MSA II horizons in cave 1 (KRM from Layer 141, KRM from Layer 14, and KRM from Layer 17 of Singer and Wymer, 1982). Although these specimens derive from horizons that may represent several discrete occupation events, all are considered to be penecontemporaneous (Rightmire and Deacon, 1991). Various skeletal elements that have been recovered from the LBS and SAS members have been claimed to demonstrate higher sexual dimorphism than living humans (Rightmire and Deacon, 1991; Bräuer et al., 1992; Lam et al., 1996; Rightmire et al., 2006). This is perhaps most apparent in the mandibular corpora from the SAS member (see Fig. 1), where there is a striking size difference between the larger specimens (KRM and 41815) and the smallest one (KRM 16424). Assuming the larger specimens to be males and the smaller one a female, Rightmire and Deacon (1991) computed indices of maximum sexual dimorphism (ratio of largest male to smallest female multiplied by 100) for corpus height and breadth at M 1 of and , respectively. Both values are much larger than the respective ratios of and for a sample of 50 South African blacks (sexes equally represented) reported by them. A similar pattern was documented for M 2 buccolingual (BL) crown diameter. There has been some debate over whether the level of variation at Klasies is driven by the inclusion of a single specimen, the KRM mandible that has been posited by Smith (1992, 1994) to represent an aberrantly small individual. Importantly, other elements such as a gracile frontal fragment and a large zygomatic (Rightmire and Deacon, 1991), as well as three metatarsals (Rightmire et al., 2006) and two maxillary fragments (Rightmire and Deacon, 1991; Bräuer et al., 1992), also provide evidence for considerable size differences among the individuals sampled in the LBS and SAS members. However, only the mandibular corpora and M 2 s are preserved in sufficient numbers and provide homologous measurements to directly test the hypothesis of greater size variation and dimorphism than in recent humans. As noted by Lam et al. (1996), the case for a high degree of sexual dimorphism at Klasies rests on the assumption that only the diminutive KRM mandible represents a female, while all of the larger specimens are male. If one (or more) of the larger mandibles is also female, then the degree of size variation attributable to sex has been overestimated. Sexual assignment of fossils based on size alone is problematic because any overlap between the male and female size ranges will result in sex misidentification, with small males being identified as females and large females being identified as males. Indeed, the techniques commonly used to estimate sexual dimorphism in fossil assemblages tend to overestimate it when the true level of dimorphism in the sample is low (Plavcan, 1994; Rehg and Leigh, 1999). One way to overcome these issues is to use the coefficient of variation (CV), a measure of size variation, in conjunction with resampling techniques such as bootstrapping (e.g., Lockwood et al., 1996; Arsuaga et al., 1997a; Lockwood, 1999; Lockwood et al., 2000; Silverman et al., 2001; Schrein, 2006). This approach permits a rigorous comparison of levels of variation between fossil and living samples and enables inferences about sexual dimorphism without reliance on the a priori sex assignment of individual specimens. The CV provides a useful approach to estimating dimorphism because as the latter increases, the separation of male and female means leads to increased intraspecific variation (Plavcan, 1994). In the present study, we use this methodology to reexamine the issue of size variation and sexual dimorphism in the Klasies assemblage. We also assess size variation in the mandibles and molars of seven other fossil samples from middle and late Pleistocene sites in Europe and western Asia. In addition to providing an evolutionary context for the interpretation of size variation at Klasies, the analysis of other Pleistocene samples allows us to infer possible changes in dimorphism in later hominin evolution, and to address the concern that the KRM mandible represents an aberrantly small individual. MATERIALS AND METHODS The magnitude of size variation in three mandibular corpus variables and one molar dimension documented in eight fossil samples was compared to the variation observed in three recent human samples using resampling analysis. Data collection protocols are outlined first, followed by a detailed description of the fossil and recent human samples, as well as the resampling methodology. Measurements Height and breadth of the mandibular corpus were measured at the level of P 4 /M 1. Height was measured perpendicular to the alveolar plane, and breadth was taken as a maximum, excluding any alveolar exostoses.

3 314 D.F. ROYER ET AL. Fig. 1. Lateral and occlusal views of the Klasies River mandibles included in this study. Illustrations by Luci Betti-Nash from high-resolution casts. The geometric mean (GM) of the corpus at P 4 /M 1 was computed from these dimensions to give an overall measure of mandibular corpus size (Mosimann, 1970). In addition, the BL crown diameter of the M 2 was recorded. Mesiodistal crown diameters were not used due to the potentially confounding influence of interproximal wear on this measurement, especially in fossil samples. Only adult individuals with fully erupted M 3 s and that exhibited no or only negligible damage or resorption of the alveolar bone and limited molar wear were measured. In the recent human samples, measurements were recorded preferentially on the left side. Measurements on fossils were taken on the side with the best preservation; however, in cases where both sides were equally well-preserved, a mean of the left and right sides was used. Samples Recent human samples. We used three geographically diverse recent human groups (Zulu, Inuit, and Nubian) composed of approximately equal numbers of males and females to broadly represent the range of size variation observed in living H. sapiens. Mandibular and dental data were collected by one of us (FEG) for a Zulu sample consisting of 40 males and 40 females housed in the Raymond A. Dart Collection, University of the Witwatersrand. The sex of the Zulu specimens was determined from cadaver records. The Inuit reference sample comprises a separate mandibular and dental data set, each represented by 25 males and 25 females sexed from associated pelves. Inuit corpus measurements were recorded by B. Richmond from Aleutian specimens housed at the United States National Museum of Natural History, Washington, DC (see Richmond and Jungers, 1995), and dental measurements were recorded by one of us (DFR) from the Point Hope specimens housed at the American Museum of Natural History, New York. The Nubian sample consists of 185 individuals from an archaeological burial context. The sex of each individual was estimated from associated pelvic remains (C. Merbs, pers. comm.). The Nubian sample includes an equal mix of males and females, plus two individuals of indeterminate sex. Nubian corpus and dental measurements were recorded by one of us (JES) and by C. Schrein from specimens housed at Arizona State University (see Scott and Lockwood, 2004). We measured sexual dimorphism in the reference samples using the index of sexual dimorphism (ISD), which is simply the ratio of the male mean to the

4 SIZE VARIATION IN PLEISTOCENE HUMANS 315 TABLE 1. Fossil samples Fossil sample Mandible sample M 2 sample Data source Klasies River KRM 13400, 16424, KRM 13400, FEG (pers. obs.) 21776, Skhūl 2, 4, 5 2, 4, 5, 7 McCown and Keith (1939) Dolní Věstonice DV 3, 13, 14, 15, 16, Pavlov 1 DV 3, 13, 14, 15, 37, Pavlov 1 Sládek et al. (2000) Sima de los Huesos AT-1, 2, 3, 75, 172, 250, 300, 505, 605, 607, 792, 950, 888, 1775 AT-250, 271, 273, 284, 300, 505, 557 Bermúdez de Castro (1993), Rosas (1997) Arago 2, 13 2, 10, 13, 32, 68, 69 Wood (1991), M. Wolpoff (pers. comm.), S. Bailey (pers. comm.), FEG (pers. obs.) Krapina Kr 54 (mandible D), Kr 55, 57, 58, 59, 1, 2, 3, Wolpoff (1979), F. Smith (pers. comm.) 55 (mandible E), 57 (mandible G), 6, 10, 83, 86, (mandible H), 59 (mandible J) Shanidar 1, 2, 4 2, 6 Trinkaus (1983) Vindija Vi 206, 226, 231 Vi 206, 231 F. Smith (pers. comm.), Wolpoff et al. (1981) female mean. These values for the M 2 were compared against published means for 32 recent human samples (Frayer and Wolpoff, 1985) to assess whether our reference samples are representative of living human dimorphism. Similarly, we compared the ISD values for the mandibular corpus against published means for two recent human samples (de Villiers, 1976; Humphrey et al., 1999). Fossil samples. The human assemblage at Klasies River includes four partial mandibles that preserve the corpus at P 4 /M 1 (see Fig. 1); these penecontemporaneous specimens were recovered from the SAS member in caves 1 and 1B (Rightmire and Deacon, 1991). The Klasies sample includes specimen KRM 16424, a right corpus with M 1 M 3 in situ that stands out from the others due to its small size and slender shape. Specimen KRM shows discoloration indicative of burning, including blackening of the M 1 crown, but there is no evidence of bone shrinkage or distortion due to fire (Singer and Wymer, 1982; Rightmire and Deacon, 1991). This specimen has suffered loss of cortical bone along the lateral and inferior aspects of the corpus, as well as damage to the M 1 crown that prevents the inclusion of this tooth in the present study. We obtained an estimated corpus breadth for KRM of mm (reconstructed estimate range: mm), which is smaller than the 13.2 mm reported by Singer and Wymer (1982: 142). At 22.4 mm, our estimate of corpus height is consistent with the original description for this measurement as slightly more than 20 mm (Singer and Wymer, 1982: 142). Three sets of analyses employing the average, minimum, and maximum values for the corpus breadth of KRM were conducted to measure corpus breadth variation at Klasies. The KRM specimen exhibits a prominent torus mandibularis at the level of the premolars and M 1 (Singer and Wymer, 1982). In order to avoid inflating mandibular breadth variation within the Klasies sample due to this feature, we used (separately) measurements taken inferior and superior to the torus. Like the Klasies assemblage, the other fossil samples selected for analysis contained roughly contemporaneous specimens from a single locality. Seven middle and late Pleistocene fossil samples, for which mandibular corpus and M 2 dimensions were available, fit these criteria: Skhūl, Dolní Věstonice, Sima de los Huesos, Arago, Krapina, Shanidar, and Vindija. Fossil data were collected by the authors on the original specimens and from published sources (McCown and Keith, 1939; Wolpoff, 1979; Wolpoff et al., 1981; Trinkaus, 1983; Wood, 1991; Bermúdez de Castro, 1993; Rosas, 1997; Sládek et al., 2000). The mandibular and molar specimens included in each fossil sample are listed in Table 1. The measurements for mandibular corpora from Skhūl, Dolní Věstonice, Sima de los Huesos, and Shanidar were taken from published sources that recorded height and breadth at the level of the mental foramen. However, these data are approximately equivalent to our own measurements, because the mental foramen typically lies at the level of P 4 /M 1. Similarly, because comparisons of variation should not be sensitive to slight differences in the point of measurement as long as data collection is consistent, we used published data on the Arago mandibles, which were measured at the level of M 1 (Wood, 1991). With the exception of the Shanidar sample, we have no a priori reason to suspect sex bias in the fossil assemblages. The Shanidar site appears to preserve the remains of both sexes, but the three Shanidar mandibles that were complete enough to be included in this study have been interpreted as belonging to males on the basis of associated cranial (Shanidar 2), pelvic (Shanidar 1 and 4), and other postcranial remains (Trinkaus, 1983). We included the Shanidar mandibles in the present study with the expectation that, as an all-male sample, it will not exceed the modern range of size variation. Summary statistics for each fossil sample are presented in Tables 2 (mandibles) and 3 (molars). Resampling analysis The sample-size-corrected CV [V* 5 (1 1 1/4n) 3 CV] was calculated for all fossil samples containing three or more specimens. This statistic permits comparison of relative variation in samples with different means, while correcting for possible bias due to small sample size (Sokal and Braumann, 1980; Sokal and Rohlf, 1995). In addition, we used the maximum/minimum ratio (MMR), which is simply the greatest value divided by the smallest value in the sample. The MMR makes no a priori assumption regarding the sex of individual specimens. Although the CV outperforms range-based measures of variation such as the MMR in simulation tests (Cope and Lacy, 1995), the MMR nonetheless provides a measure of relative size variation and permits incorporation of fossil samples that consist of only two individuals. Following Lockwood et al. (1996) and others (e.g., Arsuaga et al., 1997a; Lockwood, 1999; Lockwood et al., 2000; Silverman et al., 2001; Villmoare, 2005; Schrein,

5 316 D.F. ROYER ET AL. Fossil sample TABLE 2. Summary statistics for fossil mandibles n Mean (mm) Standard deviation V* MMR Klasies River a Height Breadth b Breadth c GM b GM c Skhūl Height Breadth GM Dolní Věstonice Height Breadth GM Sima de los Huesos Height Breadth GM Arago Height Breadth d GM Krapina Height Breadth GM Shanidar Height Breadth GM Vindija Height Breadth GM Abbreviations: V*, coefficient of variation corrected for small sample size (Sokal and Rohlf, 1995); MMR, maximum/minimum ratio; GM, geometric mean of corpus height and breadth at P 4 /M 1. a Corpus height for KRM adjusted to account for slight alveolar resorption at P 4 ; corpus breadth of KRM measured inferior to the mandibular torus. b Includes a reconstructed estimate of corpus breadth (11.25 mm) for the diminutive KRM specimen. c Includes a minimum estimate of corpus breadth (11.00 mm) for the diminutive KRM specimen. d Arago 13 mandibular torus included in corpus breadth measurement. TABLE 3. Summary statistics of M 2 BL crown diameter fossil samples Fossil sample n Mean (mm) 2006), we used bootstrapping, or resampling with replacement, to test the null hypothesis that the size variation observed in the fossil samples does not exceed that found in recent human populations. Unlike exact randomization, which considers only pairs of fossils, bootstrapping allows for the full range of variation within a sample to be considered (Cope and Lacy, 1995; Lockwood et al., 1996). Resampling analyses were conducted in Microsoft Excel VC using a macro developed by one of us (CAL; see Supporting Information). For each comparison, 10,000 samples equal in size to the fossil sample were randomly generated from each of the three recent human samples. For each iteration, V* and MMR were computed, creating six distributions (i.e., two for each recent human sample) of values by which to evaluate the variation documented in a particular fossil sample. The null hypothesis of no difference was rejected in cases where the probability of sampling the level of variation in the fossil sample from the modern human distribution was less than or equal to 5% (P 0.05). Rejection of the null hypothesis supports the alternative hypothesis of greater size variation in the fossil sample and is consistent with an interpretation of greater sexual dimorphism, although the latter is not directly tested here. We used directional tests because most studies have suggested higher levels of size variation and sexual dimorphism in middle and late Pleistocene hominins than in recent humans (see Introduction). RESULTS Modern human dimorphism Standard deviation V* MMR Klasies River Skhūl Dolní Věstonice Sima de los Huesos Arago Krapina Shanidar Vindija Abbreviations: BL, buccolingual; V*, coefficient of variation corrected for small sample size (Sokal and Rohlf, 1995); MMR, maximum/minimum ratio. Sexual dimorphism in the known-sex modern samples was quantified using the ISD, which is the ratio of the male mean to the female mean, whereas size variation within each sample is reflected in the CV and MMR (Table 4). These samples are characterized by levels of mandibular and molar dimorphism that range from 1.01 to 1.07, or 1% to 7% (Table 4). It is informative to place these three samples into the broader context of variation in human sexual dimorphism, as the selection of reference samples can affect the results of resampling-based analyses (Aiello et al., 2000). Using data from 32 globally distributed samples (Frayer and Wolpoff, 1985: Table 4, excluding samples with 10 individuals of either sex), we computed a median ISD of 1.04 (range, ) for M 2 BL crown diameter. With a median value of 1.04, the molar ISDs of our reference samples represent the central tendency in living human molar sexual dimorphism. With respect to the mandible, Humphrey et al. (1999) reported ISDs of 1.11 and 1.12, respectively, for corpus height and breadth at the level of the M 1 for a sample of 15 males and 15 females from the Spitalfields crypt in Britain. They also reported ISDs of 1.09 and 1.05 for corpus height and breadth for a sample of 30 Zulu with a near-equal sex ratio selected from the Dart Collection (University of the Witwatersrand, South Africa). Their ISD values for the Zulu sample differ from the ISDs of 1.04 for corpus height and breadth at M 1 reported by de Villiers (1976: used by Rightmire and Deacon, 1991) for a sample of 100 Zulu with an equal sex ratio. The three human samples employed in the present study provide ISDs for corpus height and breadth at P 4 /M 1 that range from 1.05 to 1.07 and 1.01 to 1.07, respectively, more or less bracketing the Zulu mandibular dimorphism reported by de Villiers. Our dimorphism values are lower than those reported by Humphrey et al. (1999) for the

6 SIZE VARIATION IN PLEISTOCENE HUMANS 317 TABLE 4. Summary statistics for recent human reference samples Reference sample Male n Female n Total n Mean (mm) Standard deviation CV MMR ISD Corpus height, P 4 /M 1 Zulu Inuit Nubian Corpus breadth, P 4 /M 1 Zulu Inuit Nubian a Corpus GM Zulu Inuit Nubian a M 2 BL Zulu Inuit Nubian Abbreviations: CV, coefficient of variation; MMR, maximum/minimum ratio; ISD, index of sexual dimorphism (male mean/female mean); corpus GM, geometric mean of corpus height and breadth at P 4 /M 1 ; BL, buccolingual crown diameter. a Includes two specimens of indeterminate sex. Zulu and Spitalfields samples. Differences in sample size, sample composition, and measurement protocol may account for the divergent Zulu ISD values. The three Zulu samples are not fully independent since all were selected from the Dart Collection (University of the Witwatersrand, South Africa). However, given the large size of the Dart Collection, it is unlikely that the same individuals were included in all of the studies, although this cannot be confirmed because specimen numbers were not published. When we compare the range of MMR in our three samples (corpus height ; corpus breadth ) with the Spitalfields MMR (corpus height ; corpus breadth ) reported by Humphrey et al. (1999), it is clear that our samples exhibit a range of mandibular size variation that encompasses the European variation. Thus, the Zulu, Inuit, and Nubian samples selected for this analysis appear to be appropriate models against which to compare mandibular size variation in hominin fossils. Size variation in late Pleistocene fossils Klasies River. In terms of the mandibular corpus GM, the Klasies River fossils are significantly more variable than the three recent human reference samples employed here, regardless of whether variation is computed as V* or MMR (Table 5). If mandibular corpus height is considered separately, the Klasies sample also exhibits significantly greater size variation than the recent human samples using both V* and MMR as indicators of variation. That is, there is less than a 5% probability of sampling a Klasies level of variation (V* , MMR ) among the recent human samples (Fig. 2; Table 5). However, size variation in corpus breadth is not significantly greater than in the recent samples (Table 5). These bootstrap results use the average breadth estimate for the reconstructed diminutive KRM specimen (11.25 mm); however, the results for corpus breadth are also statistically nonsignificant using the minimum (11.0 mm) and maximum (11.5 mm) reconstructed breadths for this specimen. Similarly, the results are nonsignificant regardless of whether KRM is measured superior or inferior to the mandibular torus. The Klasies M 2 sample also shows significantly greater variation in the M 2 BL diameter than in all three recent samples (Table 5). Skhūl. With regard to the mandibular corpus GM, the Skhūl sample shows significantly greater size variation (V* and MMR) than either the Inuit or Nubians. Compared to the Zulu, there is only a 3.66% probability of sampling an MMR greater than that of Skhūl (MMR ), but there is slightly higher probability (5.34%) of sampling a V* greater than Skhūl (V* ) (Table 5). Variation in corpus height among the Skhūl mandibles is significantly greater than that in the three recent human samples (Fig. 2; Table 5); however, size variation in corpus breadth does not differ significantly from that in the reference samples. The Skhūl M 2 sample also does not exhibit significantly more size variation than recent humans (Table 5). Dolní Věstonice. The six mandibles from Dolní Věstonice do not display significantly greater size variation than any recent human sample for corpus GM and corpus breadth. However, when corpus height alone is considered, the Dolní Věstonice mandibles show a significantly greater degree of size variation (V* and MMR) compared to the Zulu, Inuit, and Nubian samples (Fig. 2; Table 5). The M 2 s from Dolní Věstonice do not display significantly greater size variation compared to the recent humans regardless of whether V* or MMR is used (Table 5). Krapina, Shanidar, and Vindija. None of the Neandertal samples exhibit significantly greater size variation in mandibular corpus height or breadth than any of the recent human reference samples (Fig. 3; Table 5). When the GM of the corpus is considered, the probability of sampling a V* as high as that for Krapina (V* ) from the Inuit sample is low (2.05%), but the sample does not differ significantly from the Zulu and Nubian samples. Similarly, the Vindija mandibles show significantly greater variation in corpus GM compared to the Inuit, but not the Zulu and Nubians (Table 5). For M 2 BL diameter, the Krapina assemblage exhibits levels of variation within the range of the reference samples, except when compared to the Inuit MMR resampled distribution (Table 5). Neither the Vindija nor the Shanidar

7 318 D.F. ROYER ET AL. TABLE 5. Bootstrap results mandibular corpus at P 4 /M 1 and M 2 BL crown diameter vs. Zulu vs. Inuit vs. Nubian Fossil sample V* MMR V* MMR V* MMR Corpus height Klasies River Skhūl Dolní Věstonice Sima de los Huesos Arago Krapina Shanidar Vindija Corpus breadth Klasies River a Skhūl Dolní Věstonice Sima de los Huesos Arago Krapina Shanidar Vindija Corpus GM Klasies River a Skhūl Dolní Věstonice Sima de los Huesos Arago Krapina Shanidar Vindija M 2 BL Klasies River Skhūl Dolní Věstonice Sima de los Huesos Arago Krapina Shanidar Vindija Abbreviations: BL, buccolingual; V*, coefficient of variation corrected for small sample size; MMR, maximum-minimum ratio; corpus GM, geometric mean of corpus height and breadth at P 4 /M 1. Significant values (P \ 0.05) are in bold. a Sample includes the reconstructed estimate of corpus breadth for the diminutive KRM specimen and measurement of KRM taken inferior to torus; all results are equivalent using the minimum estimate for KRM and measuring specimen KRM superior to torus. M 2 samples show greater size variation compared to any of the recent human samples. Size variation in middle Pleistocene fossils Sima de los Huesos. The 14 mandibles from Sima de los Huesos do not exhibit significantly greater variation in corpus GM and corpus breadth than the Zulu, Inuit, and Nubian samples. However, these mandibles show significantly greater variation in corpus height compared to recent humans (Fig. 3; Table 5). The Sima de los Huesos M 2 sample is not significantly more variable than any of the recent human samples (Table 5). Arago. Since the Arago sample includes only two mandibles, resampling was limited to comparisons of MMR. The GM and corpus breadth analyses show significantly greater size variation in the Arago sample than the Inuit, but not the Zulu or Nubians (though the probabilities for corpus breadth approach significance; Table 5). In corpus height, the Arago sample is not significantly greater than any of our modern samples, while the M 2 sample from this site exhibits significantly greater size variation than all of the human reference samples (although using the MMR, Arago only approaches significance compared to the Nubians; Table 5). DISCUSSION Methodological considerations We used three different variables in the analysis of mandibular size variation in recent and middle and late Pleistocene Homo: the height and breadth of the mandible at P 4 /M 1, and the geometric mean of these two dimensions. We compared magnitudes of size variation to make inferences regarding changes in sexual dimorphism in past human populations, although dimorphism was not directly examined. Some recent analyses of mandibular size variation and dimorphism have focused mainly on the GM (e.g., Richmond and Jungers, 1995; Lockwood et al., 1996; Silverman et al., 2001). However, several studies have shown that sexual dimorphism has a complex expression throughout the skeleton (Wood,

8 SIZE VARIATION IN PLEISTOCENE HUMANS 319 Fig. 2. Coefficients of variation (V*) for the Skhūl (top), Klasies River (middle), and Dolní Věstonice (bottom) samples compared to those generated from bootstrapping the Zulu sample. Note that the Zulu distributions differ in each case because the sample sizes for the fossil samples differ (Skhūl, n 5 3; Klasies, n 5 4; Dolní Věstonice, n 5 6; see text for further details). Size variation in each fossil sample is statistically significantly higher than the extant human comparative values. Fig. 3. Coefficients of variation (V*) for the Sima de los Huesos (top), Krapina (middle), and Vindija (bottom) samples compared to those generated from bootstrapping the Zulu sample. Note that the Zulu distributions differ in each case because the sample sizes for the fossil samples differ (Sima de los Huesos, n 5 14; Krapina, n 5 5; Vindija, n 5 3; see text for further details). Only the Sima de los Huesos variation is statistically significantly higher than the extant human comparative values. 1976, 1985; Oxnard, 1987; O Higgins et al., 1990; Lockwood, 1999; Plavcan, 2001, 2002). For example, in anthropoids, including humans, the neurocranium tends to show less dimorphism than aspects of the face and mandible (de Villiers, 1968; Plavcan, 2002). Among indigenous South Africans, de Villiers (1968) documented greater dimorphism in the mandible compared to other aspects of the skull, and subsequent studies have identified differences in the expression and magnitude of dimorphism of this element among closely related Bantu-speaking South African groups (Franklin et al., 2008a,b) and other human populations (Humphrey et al., 1999). The variable expression of dimorphism is not limited to the mandible, with Oxnard (1987) having documented differences in both magnitude and pattern between mandibular and maxillary teeth in humans and apes. Differences in the magnitude of sexual dimorphism among anatomically proximate regions, such as the mandible and molar dentition, and even in different measurements of the mandible, are also apparent in the present study. These results highlight the fact that the use of a composite measurement, such as the GM, in estimates of size variation and dimorphism can obscure differences in the individual measurements that constitute it. For this reason, we limit our discussion to separate height and breadth dimensions of the mandibular corpus. A second methodological issue that warrants discussion is the interpretation of statistically nonsignificant differences between the fossil and recent human samples. In the present study, failure to reject the null hypothesis of equivalent relative variation in the extant and the fossil samples can be interpreted in three ways: (1) the populations represented by the samples are very similar in their levels of size variation (and by inference, sexual dimorphism); (2) the sex ratio of the fossil sample

9 320 D.F. ROYER ET AL. is biased, leading to an artificially low level of variation (see also Scott and Stroik, 2006); or (3) the variation in the fossil sample is statistically indistinguishable from that in extant humans because the fossil sample is too small to provide an adequate estimation of population variation (and by inference, sexual dimorphism). These factors, which are not mutually exclusive, may pertain to our interpretation of the statistically nonsignificant results from the three Neandertal assemblages. In particular, the size of some of the Neandertal samples is a concern. As noted previously, in the case of the Shanidar corpus sample (but not the molar sample), we can implicate a biased sex ratio as the cause of low variation. For the molars, at least one of the Neandertal samples (Krapina) contains a reasonably large number of specimens (n 5 12). Thus, it seems unlikely that small sample size fully accounts for failure to reject the null hypothesis in all three Neandertal molar samples and for the two mandibular samples for which there is no evidence of significant sex bias. Nevertheless, given the issues described earlier, it is important to point out that our interpretation of these nonsignificant results should be considered provisional and subject to revision based on analyses of expanded fossil samples. Implications for sexual dimorphism in the middle and late Pleistocene To the extent that size variation can be used as a proxy for sexual dimorphism, the resampling results presented here support previous conclusions that the Klasies River sample is characterized by a higher degree of mandibular and dental sexual dimorphism than modern humans (Rightmire and Deacon, 1991; Bräuer et al., 1992; Lam et al., 1996). Whether these differences in gnathic and dental dimorphism between the Klasies and recent humans indicate greater overall body size dimorphism in the former remains unclear, but it is reasonable to hypothesize such a relationship (Plavcan, 2003). Although the Klasies fossils are generally attributed to H. sapiens (e.g., Bräuer, 1984; Rightmire, 1984), this assemblage is morphologically diverse and not uniformly modern in character (Trinkaus, 2005). For example, the mandibles have a variable expression of the chin, ranging from incipient to one indistinguishable from those of living humans (Frayer et al., 1993; Lam et al., 1996), and aspects of the proximal ulna and radius display a mixture of archaic and modern morphologies (Churchill et al., 1996; Pearson and Grine, 1997; Pearson et al., 1998). The archaic versus modern nature of an isolated zygomatic has been the subject of debate (Smith, 1992; Frayer et al., 1993; Smith, 1994; Bräuer and Singer, 1996a,b; Wolpoff and Caspari, 1996), and a frontal fragment that bears a gracile supraorbital region and glabella has been argued to represent an adolescent, raising the possibility that the adult morphology might be more robust and archaic in appearance (Smith, 1992, 1994). Concomitant with the presence of some archaic morphologies, the mandibular and molar elements from Klasies also exhibit a level of size variation and probably dimorphism that is beyond that of recent humans. Although there is uncertainty regarding the true age of the Skhūl fossils (Millard, 2008), with uranium-series and ESR dates converging on 100 ka (Stringer et al., 1989; McDermott et al., 1993) and thermoluminescence dating pointing to a slightly older age (ca. 119 ka) for the Near Eastern skeletons (Mercier et al., 1993), the available evidence suggests that these fossils may be broadly contemporaneous with the Klasies assemblage. McCown and Keith (1939: 13) observed variation within the Skhūl specimens to be greater in degree and kind than is to be observed in any local community of modern times. They did not invoke sexual dimorphism as the cause of this variation, but rather suggested an evolutionary transition or hybridization as the cause. It is clear from the long bones that this assemblage includes both large (probable male) and very small (probable female) adults (McCown and Keith, 1939). Our results indicate that the Skhūl fossils exhibit the same pattern of mandibular variation observed at Klasies, where corpus height shows a greater range of size variation but corpus breadth is within the range expressed by recent groups. The same pattern of mandibular corpus size variation is also observed in the Dolní Věstonice sample, which is radiocarbon-dated to ka (Sládek et al., 2000). Although not directly tested here, these results are consistent with an interpretation of higher levels of mandibular sexual dimorphism in the Dolní Věstonice, Skhūl, and Klasies River populations and suggests a fairly recent reduction in dimorphism to current levels in our species. Importantly, the Skhūl and Dolní Věstonice results also indicate that the high level of size variation in the Klasies sample is not unusual among late Pleistocene hominins. Thus, while KRM is indeed small, its inclusion in the Klasies sample does not produce an anomalous level of size variation for a sample of this geologic age. In light of these findings, it is not necessary to consider this specimen as an aberration and exclude it from consideration (Smith, 1992, 1994). The molar analyses present a different picture: while Klasies exhibits greater M 2 size variation than recent populations, variation in the Skhūl and Dolní Věstonice samples does not differ from that observed today. Thus, purported H. sapiens populations from the late Pleistocene appear to have differed from one another in the expression of sexual dimorphism, and within our species, reduction in dimorphism would seem to have occurred in a mosaic fashion in the molars and the mandible. With respect to the Krapina, Shanidar, and Vindija samples, our study documents a shared pattern of mandibular size variation among these Neandertals groups. All exhibit low levels of variation in mandibular corpus height and breadth. In the case of the Shanidar fossils, low mandibular size variation is not surprising since the sample is believed to contain only males (Trinkaus, 1983). Notably, the Krapina results do not support Smith s (1976) suggestion of high mandibular variation/ dimorphism in this paleopopulation. The Neandertal M 2 samples also exhibit size variation that fits comfortably within the recent human range. These results are consistent with the hypothesis that Neandertals were characterized by low levels of sexual dimorphism (comparable to recent populations) in their mandibles and molars. As noted earlier, our conclusions should be considered tentative given that most of the Neandertal samples comprise less than six specimens. However, this interpretation accords with previous work by Trinkaus (1980), who documented levels of postcranial dimorphism indistinguishable from those of modern populations in both single-site Neandertal samples (e.g., Krapina) and across the spectrum of European and Near Eastern specimens in analyses of Neandertal skeletons sexed on the basis of pelvic morphology. Research suggesting greater cranial dimorphism among Neandertals (Smith, 1980) may

10 SIZE VARIATION IN PLEISTOCENE HUMANS 321 have been influenced by analyses of a geographically and temporally mixed sample of presumed males and females. Like the Klasies River, Skhūl, and Dolní Věstonice samples, the fossils from Sima de los Huesos exhibit greater variation in corpus height than the recent human populations, and this may be attributable to sexual dimorphism. Rosas et al. (2002) also documented greater dimorphism in various aspects of the mandibles from Sima de los Huesos, including corpus height, although their assessment of dimorphism was based on a priori sex assignments of the fossils. However, the present study demonstrates that the size variation in corpus breadth in the Sima de los Huesos sample lies within the range observed in the modern groups. Similarly, the bootstrap analyses by Arsuaga et al. (1997a; see also Lorenzo et al., 1998) for several postcranial dimensions and cranial capacity also suggest comparable levels of dimorphism between the Sima de los Huesos sample and living humans. Bootstrap analyses conducted by Bermúdez de Castro et al. (2001) demonstrated that variation in the crown areas of the Sima de los Huesos M 1 s and M 2 s is within the range observed in a sample of modern Portuguese, although the lower canines and P 4 s from this site were found to exhibit significantly higher variation than their recent human sample. Our results provide further evidence that the magnitude of molar size variation in the Sima de los Huesos fossils is within the range of modern humans. On the other hand, Bermúdez de Castro and colleagues (1993, 2001) concluded that sexual dimorphism in the Sima de los Huesos molars was greater than in modern humans based on ISDs calculated using specimens they had sexed on the basis of size. However, given that sex assignments based on size will overestimate dimorphism in a population in which there is overlap between male and female ranges, we are skeptical of these results and would instead submit that there is no evidence for higher-than-modern size variation and thus sexual dimorphism in the Sima de los Huesos molars. Taken with the evidence for greater size variation in mandibular corpus height, but not in other cranial or postcranial dimensions (Arsuaga et al., 1997a; Lorenzo et al., 1998), it appears that the Sima de los Huesos population was similar to modern humans in its overall degree of skeletal dimorphism, although it was not identical. Some features (e.g., corpus height, canine and P 4 crown areas) appear to have demonstrably greater size variation and possibly higher-than-modern sexual dimorphism. These results may highlight the complex expression of dimorphism in the skeleton. Our bootstrap analyses do not allow us to reject the hypothesis that the Arago mandibular sample is similar to modern humans in its level of size variation and, by inference, sexual dimorphism. For corpus breadth, the magnitude of variation in the Arago sample is influenced by the presence of a mandibular torus in Arago 13 (Wood, 1991). Even so, the Arago mandibles exhibit greater size variation only in comparison with the Inuit, a modern group that exhibits essentially no dimorphism in corpus breadth. With respect to M 2 BL diameter, Arago exhibits significantly greater variation than in the recent human samples, suggesting greater dimorphism than in recent humans. At n 5 2, the Arago fossils constitute the smallest mandibular sample in the analysis, and thus the statistically nonsignificant results may be influenced by other factors, as previously discussed. Since the molar sample includes four isolated teeth in addition to the two associated with the mandibles, there is a strong possibility that our divergent results for the variation in the Arago mandibles and M 2 s are simply the product of a larger dental sample. Interestingly, when the analysis is limited to the Arago 2 and Arago 13 molar specimens (MMR ), variation remains significantly higher than in the recent humans (Zulu, P ; Inuit, P ; Nubian, P ). The relatively high degree of size variation in corpus height observed at Klasies River, Skhūl, and Dolní Věstonice, as well as in the Sima de los Huesos sample attributed to H. heidelbergensis and considered by many to be directly ancestral to Neandertals (e.g., Arsuaga et al., 1997b; Rightmire, 1998, 2008), raises the possibility that the recent human and Neandertal low levels of dimorphism in corpus height may have developed independently and at different times. The presence of comparatively high variation in the Klasies M 2 sample and low variation in the geologically older Sima de los Huesos M 2 s is consistent with this hypothesis. However, as previously noted, the fact that we are drawing this inference from small fossil samples means that more material is needed to test this hypothesis. CONCLUSIONS This study demonstrates that size variation in the Klasies River mandibular and dental samples is greater than in modern human populations, supporting the hypothesis that this MSA population was more dimorphic in some aspects of its skeleton than living humans. High levels of mandibular variation specifically in corpus height are also characteristic of the Skhūl, Dolní Věstonice, and Sima de los Huesos samples. To the extent that size variation can be used as a proxy for sexual dimorphism, these results suggest that the degree of dimorphism exhibited in the Klasies specimens was not unique among middle and late Pleistocene hominins. In contrast, there is little evidence for high levels of mandibular or molar size variation among samples of Neandertals. A reduction in sexual dimorphism may have occurred independently in the modern human and Neandertal lineages, with a more recent reduction in variation and sexual dimorphism in the former occurring after ka. ACKNOWLEDGMENTS We thank Brian Richmond and Caitlin Schrein for the use of their data on recent humans, Shara Bailey and Milford Wolpoff for the use of their data on the Arago molars, Fred Smith for the use of his data on the Krapina mandibles, the Department of Anatomical Sciences, University of the Witwatersrand for access to the Raymond A. Dart Collection, and Gisselle Garcia at the American Museum of Natural History for access to the Point Hope Inuit Collection. We also thank Luci Betti- Nash for her artistic rendition of the Klasies River mandibles. This paper benefited from discussions with Mike Plavcan and Liz St. Clair, as well as the helpful suggestions provided by the reviewers. LITERATURE CITED Aiello LC, Collard M, Thackeray JF, Wood BA Assessing exact randomization-based methods for determining the taxonomic significance of variability in the human fossil record. S Afr J Sci 96: