Alternative Models for Evaluating Variation and Sexual Dimorphism in Fossil Hominoid Samples Jeremiah E

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 140:253–264 (2009)

Beyond Gorilla and Pongo: Alternative Models for Evaluating Variation and Sexual Dimorphism in Fossil Hominoid Samples Jeremiah E. Scott,1* Caitlin M. Schrein,1 and Jay Kelley2

1School of Human Evolution and Social Change, Institute of Human Origins, Arizona State University, Tempe, AZ 85287-4101 2Department of Oral Biology, College of Dentistry, University of Illinois at Chicago, Chicago, IL 60612

KEY WORDS bootstrap; dental variation; Lufengpithecus; Ouranopithecus; Sivapithecus

ABSTRACT Sexual size dimorphism in the postca- cies. Using these samples, we also evaluated molar dimor- nine dentition of the late Miocene hominoid Lufengpithe- phism and taxonomic composition in two other Miocene cus lufengensis exceeds that in Pongo pygmaeus, demon- ape samples—Ouranopithecus macedoniensis from strating that the maximum degree of molar size dimor- Greece, specimens of which can be sexed based on associ- phism in apes is not represented among the extant ated canines and P3s, and the Sivapithecus sample from Hominoidea. It has not been established, however, that Haritalyangar, India. Ouranopithecus is more dimorphic the molars of Pongo are more dimorphic than those of than the extant taxa but is similar to Lufengpithecus, any other living primate. In this study, we used resam- demonstrating that the level of molar dimorphism pling-based methods to compare molar dimorphism in required for the Greek fossil sample under the single-spe- Gorilla, Pongo,andLufengpithecus to that in the papio- cies taxonomy is not unprecedented when the compara- nin Mandrillus leucophaeus to test two hypotheses: tive framework is expanded to include extinct primates. (1) Pongo possesses the most size-dimorphic molars In contrast, the Haritalyangar Sivapithecus sample, if among living primates and (2) molar size dimorphism in it represents a single species, exhibits substantially Lufengpithecus is greater than that in the most dimorphic greater molar dimorphism than does Lufengpithecus. living primates. Our results show that M. leucophaeus Given these results, the taxonomic status of this sample exceeds great apes in its overall level of dimorphism and remains equivocal. Am J Phys Anthropol 140:253–264, that L. lufengensis is more dimorphic than the extant spe- 2009. VC 2009 Wiley-Liss, Inc.

A frequently encountered problem in hominoid paleon- However, adopting a multiple-species taxonomy for a fos- tology is identification of the source of high levels of size sil sample solely on the basis of excessive size variation variation in a fossil sample (e.g., Kay 1982a,b; Lieber- relative to Gorilla and Pongo is problematic for two rea- man et al., 1988; Cope and Lacy, 1992; Albrecht and sons. First, it is not clear that the upper limit of intra- Miller, 1993; Kramer, 1993; Martin and Andrews, 1993; specific variation in extant primates is represented by Richmond and Jungers, 1995; Lockwood et al., 1996, these taxa. Among living primates, Gorilla and Pongo 2000; Plavcan and Cope, 2001; Silverman et al., 2001; are exceeded in body-mass dimorphism (and presumably Scott and Lockwood, 2004; Villmoare, 2005). While some intraspecific variation in body mass) by the African sources are relatively easily identified and controlled papionin Mandrillus sphinx (Jungers and Smith, 1997; (e.g., variation due to ontogeny or pathology), others Setchell et al., 2001). Although it has not been estab- present greater difficulty. For example, high variation in lished whether this difference is reflected in aspects of a single fossil sample can be interpreted as evidence of skeletal or dental size variation and dimorphism, data the presence of multiple species, changes in size over from other papionins, particularly Papio, indicate that at time, or marked sexual dimorphism, or some combina- least some of the members of this clade may be more tion of these factors. Determining which of these alterna- skeletally and dentally dimorphic than the great apes tives is responsible for the pattern of variation in a given (e.g., Wood, 1976; Uchida, 1996a,b; Plavcan, 2002, 2003). fossil assemblage is important because each has different Second, the upper limit of intraspecific variation may implications regarding species diversity, modes of evolu- not be represented by any extant primate. Among fossil tionary change (i.e., anagenesis vs. cladogenesis), and primates, the hominoid sample from the late Miocene social behavior. One perspective on fossil hominoid taxonomy specifies that the degree of variation in extinct species should not *Correspondence to: Jeremiah E. Scott, School of Human Evolution be greater than that in Gorilla and Pongo, the most sex- and Social Change, Institute of Human Origins, Arizona State Univer- ually dimorphic extant hominoids, which logically sity, Tempe, AZ 85287-4101, USA. E-mail: [email protected] requires rejection of a single-species hypothesis in cases where a temporally and geographically restricted fossil Received 3 July 2008; accepted 28 January 2009 sample is more variable than these great apes (e.g., Kay, 1982a,b; Lieberman et al., 1988; Martin and Andrews DOI 10.1002/ajpa.21059 et al., 1993; Teaford et al., 1993; Walker et al., 1993; see Published online 8 April 2009 in Wiley InterScience also Cope and Lacy, 1992; Cope, 1993; Plavcan, 1993). (www.interscience.wiley.com).

VC 2009 WILEY-LISS, INC. 254 J.E. SCOTT ET AL. site of Lufeng, China, represents a single species— time represented by the hominoid-bearing deposits at Lufengpithecus lufengensis—that exceeds Gorilla and Lufeng is unknown, temporal variation is unlikely to be Pongo in its degree of postcanine sexual dimorphism a major component of the high level of size variation in (Kelley and Xu, 1991; Kelley, 1993; Kelley and Plavcan, L. lufengensis, given that intrasexual variation in the 1998). Establishing that the Lufeng sample represents a sample is within the range of modern species (Kelley single highly dimorphic species was made possible by and Plavcan, 1998). The fact that L. lufengensis exceeds two key characteristics of the assemblage: the sample is Pongo in its level of molar dimorphism means that it is large, comprising hundreds of teeth (e.g., Kelley and potentially more dimorphic in the molar dentition than Etler, 1989; Wood and Xu, 1991), and a number of post- any extant primate, as Pongo is commonly thought to canine dentitions have been confidently sexed using possess the greatest level of molar dimorphism among associated canines and P3s (e.g., Kelley and Xu, 1991; living primates (e.g., Mahler, 1973; Kelley and Xu, 1991; Kelley, 1993; Kelley, 1995a,b). Using the sexed specimens Kelley and Plavcan, 1998). If true, then including the (n 16 for each molar position), Kelley and colleagues Lufeng sample as part of the comparative framework for (Kelley and Xu, 1991; Kelley, 1993; Kelley and Plavcan, assessing variation in fossil primate samples becomes 1998) demonstrated that molar dimorphism in L. lufen- even more critical. gensis is so high that there is no overlap between male In fact, it has not been quantitatively verified that and female individuals in bivariate plots of mesiodistal Pongo expresses the greatest degree of molar dimor- and buccolingual dimensions. Several researchers have phism among living primates, and therefore the claim argued that the Lufeng sample contains multiple species that the degree of molar dimorphism documented in L. (e.g., Wu and Oxnard, 1983a,b; Martin, 1991; Cope and lufengensis falls outside the range observed in living pri- Lacy, 1992; Plavcan, 1993), but a mixture of two or more mate species has not been adequately tested. Thus, in species is unlikely to have produced the pattern of varia- this study, we test two hypotheses regarding molar size tion observed in the sample, unless one appeals to highly dimorphism in primates: (1) Pongo represents the upper- improbable sampling events (Kelley and Plavcan, 1998). most extreme of molar dimorphism among living pri- Thus, L. lufengensis extends the known range of intra- mates, and (2) molar dimorphism in L. lufengensis is specific size variation and sexual dimorphism in greater than that in the most dimorphic living primate the Hominoidea, at least with respect to the postcanine species. We then apply the results of these analyses to dentition. other potential instances of extreme dimorphism in the Despite initial objections based on both ontological and late Miocene hominoid fossil record—the Sivapithecus epistemological grounds (e.g., Ruff et al., 1989; Martin, material from Haritalyangar, India, and the Ouranopi- 1991; Cope and Lacy, 1992; Martin and Andrews, 1993; thecus macedoniensis material from Greece (Kelley, Plavcan, 1993; Teaford et al., 1993; Walker et al., 1993), 2005; Schrein, 2006). Specifically, we evaluate whether the idea that some fossil hominoid species were more levels of apparent sexual dimorphism (i.e., the level of dimorphic than living great apes has gained wider accep- dimorphism required if the distinct large and small size tance, and many researchers now acknowledge extreme clusters evident in the Sivapithecus and O. macedonien- dimorphism as a potential source of high measures of sis molar samples represent conspecific males and variation that must be considered when evaluating fossil females, respectively) in these fossil samples fall within samples (e.g., Plavcan, 2001; Plavcan and Cope, 2001; the limits of dimorphism established for living primates Scott and Lockwood, 2004; Schrein, 2006; Skinner et al., and L. lufengensis. 2006; Simons et al., 2007; Humphrey and Andrews, 2008).1 This is not to say that extreme dimorphism should be regarded as the null hypothesis for Miocene hominoids; rather, we are suggesting that extreme MATERIALS AND METHODS dimorphism is a viable alternative to the hypothesis that Three extant species were included in the analysis: high levels of size variation in a fossil sample indicate the western lowland gorilla (Gorilla gorilla), the Bor- the presence of multiple species. Acceptance of L. lufen- nean orangutan (Pongo pygmaeus), and the drill (Man- gensis as a single highly dimorphic species highlights drillus leucophaeus) (Table 1). The drill was chosen to the need to incorporate other comparative species—in represent papionins because Plavcan’s (1990) data set addition to the living great apes—when evaluating fossil indicates that Mandrillus probably has the most dimor- samples. One option is to use the highly dimorphic phic postcanine teeth of any extant papionin. Mandrillus papionins as analogues, which some studies have done leucophaeus is smaller in body size than M. sphinx and (e.g., Ruff et al., 1989; Teaford et al., 1993; Uchida may not be as sexually dimorphic in body mass (Jungers 1996b; Harvati et al., 2004; Baab, 2008). Another option and Smith, 1997), but the two species have similar is to use L. lufengensis as an analogue (Kelley, 2005). degrees of postcanine dimorphism. This assessment is The use of fossil species to model intraspecific varia- based on a comparison of Plavcan’s (1990) M. leuco- tion in other fossil assemblages was suggested by Wood phaeus data set to unpublished data for M. sphinx col- (1991), who used Australopithecus boisei to determine lected by S. Frost, R. Nuger, and M. Singleton. The whether variation in A. africanus and A. robustus indi- M. leucophaeus data were used in order to avoid the cated the presence of multiple species in each of these potential for interobserver error in the M. sphinx data. hypodigms (for other examples of the use of extinct spe- For each of the extant species, maximum length (mesio- cies to evaluate variation in fossil samples, see Kelley, distal, MD) and width (buccolingual, BL) dimensions of 2005; Skinner et al., 2006; Baab, 2008). Although Wood’s the mandibular molars were taken from the literature (1991) intent in taking this approach was to control for (for G. gorilla: Mahler, 1973; for P. pygmaeus and M. leu- temporal variation, the purpose of using L. lufengensis cophaeus: Plavcan, 1990). Maxillary molars were not as an analogue would be to include a reference sample included in the analysis because sample sizes for these that possesses a level of intraspecific variation not repre- teeth are not as large as those for the mandibular sented among extant hominoids. Although the amount of molars in the fossil samples.

American Journal of Physical Anthropology MODELING SEXUAL DIMORPHISM IN MIOCENE APES 255

TABLE 1. Sample sizes for the extant comparative taxa and Thus, multivariate molar size dimorphism can be cal- L. lufengensis culated in two ways. The ﬁrst way is to calculate the ratio of GMs. For each sex, a measure of multivariate M1 M2 M3 molar size can be computed as follows: Male Female Male Female Male Female

G. gorilla 43 43 40 40 34 34 1=n GM# ¼ðGM# 3 GM# 3 ... 3 GM# Þ ; ð2Þ P. pygmaeus 20 20 20 20 18 18 ALL 1 2 n M. leucophaeus 23 18 24 18 24 16 L. lufengensis 10 12 11 11 6 10 where GM#1 is the geometric mean of M1,M2, and M3 1/3 size [i.e., (M1 3 M2 3 M3) ] for the first male, GM#2 is Data are from the following sources: G. gorilla, Mahler (1973); the geometric mean of M ,M, and M size for the sec- P. pygmaeus, Plavcan (1990); M. leucophaeus, Plavcan (1990); 1 2 3 ond male, etc., and thus GM# is the geometric mean L. lufengensis, provided by Xu Qinghua. ALL of the geometric means of all male individuals. The female geometric mean (GM$ALL) is computed in the The L. lufengensis sample is identical to the one used same way. The index of sexual dimorphism (ISD) for by Kelley and Plavcan (1998; Table 1), with the excep- multivariate molar size can then be calculated as ISD 5 tion of one additional female M3 (identified by JK after GM#ALL/GM$ALL (i.e., the ratio of GMs). reexamining the Lufeng data). This sample includes only The second way to calculate multivariate molar size molars from associated dentitions, thus making tooth dimorphism is to use the GM of ratios: position (i.e., M1,M2,M3) unambiguous and making it possible to sex teeth using associated canines and P s 1=3 3 ISD ¼ðM1 3 M2 3 M3 Þ ; ð3Þ (see Kelley, 1993). These two factors are important for ISD ISD ISD obtaining an accurate estimation of sexual dimorphism in L. lufengensis (Kelley and Plavcan, 1998). Inclusion of where M1ISD is the ISD for M1 (i.e., mean M1 size for isolated and unsexed molars has the potential to bias males divided by mean M1 size for females), M2ISD is estimates of dimorphism upwards, either by mixing M s the ISD for M2, and M3ISD is the ISD for M3. Note that 1 Equations 3 and 1 are equivalent. and M2s or by including large females in the male sample and small males in the female sample (e.g., Kelley When using the ratio of GMs (i.e., GM#ALL/GM$ALL)to and Etler, 1989; Kelley and Plavcan, 1998). calculate multivariate molar size dimorphism, all of the Sexual dimorphism in Lufengpithecus lufengensis and specimens in the analysis must possess each molar; the extant species, quantified using log-transformed those lacking one or more molars must be excluded. However, using the GM of ratios [i.e., (M1ISD 3 M2ISD 3 (base e) indices of sexual dimorphism (following Smith, 1/3 1999), was compared in two ways: (1) by combining the M3ISD) ], specimens with missing data can be retained individual molars into a single measure (i.e., multivari- because the ISD for each molar position is calculated in- ate molar size dimorphism) and (2) by analyzing each dependently of the other positions (Gordon et al., 2008), molar position separately. This allowed us to evaluate and thus fossil specimens that do not preserve the entire overall dimorphism in the molar row and to account for molar row can be included in the analysis. For this the fact that comparisons among individual teeth are not study, the GM of ratios was used to calculate ISDs for independent (i.e., species with highly dimorphic M s are each sample in order to account for the fact that within- 1 sex sample sizes for each molar position were not equal also likely to have highly dimorphic M2s), while also examining the differences at each molar position. For for any of the species or fossil samples used in the analy- both analyses, molar size was represented by the geo- sis (Table 1). metric mean of the MD and BL dimensions [i.e., (MD 3 To statistically evaluate differences between sample BL)1/2]. ISDs, we used the bootstrap (i.e., resampling with For the analysis of multivariate molar size dimor- replacement) to generate 95% confidence intervals for phism, we used the geometric-mean-based method devel- each pairwise difference as follows: oped by Gordon et al. (2008), which is useful for examining the overall dimorphism in a series of variables 1. For each molar position, Sample A (e.g., G. gorilla) (molar dimensions in this case) and has the benefit that was resampled with replacement 2000 times,2 with specimens with missing data (e.g., incomplete fossil the sample size and sex ratio for each bootstrap sam- specimens) can be included. This approach takes advan- ple being identical to those of the original sample. tage of the fact that the ratio of two geometric means is Note that, because we resampled with replacement, a mathematically equivalent to the geometric mean of the specimen could be included in each bootstrap sample individual ratios for each of the variables that constitute multiple times or not included at all, and thus each the geometric means (Gordon et al., 2008): iteration was highly unlikely to produce a sample that was identical to the original sample in specimen h i composition. GM x y z 1=3 2. The ISD for each bootstrap sample was then com- 1 ¼ 1 3 1 3 1 ; ð1Þ GM2 x2 y2 z2 puted. For the analysis of multivariate molar size dimorphism, bootstrap samples for each molar position were randomly grouped together (i.e., one boot- where GM1 is the geometric mean of the means (i.e., the strap sample of M1s, one bootstrap sample of M2s, cube root of the product of x1, y1, and z1) for a set of vari- and one bootstrap sample of M3s), and multivariate ables measured on individuals in Group 1 (e.g., males of molar dimorphism was calculated as the GM mean of a particular species) and GM2 is the geometric mean of the ISDs for each molar position. Note that we did the means for the same set of variables (i.e., x2, y2, and not resample entire molar rows at once. Thus, in the z2) measured on individuals in Group 2 (e.g., females of case of the G. gorilla sample, for each iteration, an the same species). M1 ISD calculated using 43 males and 43 females was

American Journal of Physical Anthropology 256 J.E. SCOTT ET AL. between Sample A and Sample B (disregarding the sign of the difference). 3. Finally, we divided the value obtained from Step 2 by the total number of bootstrap samples. The observed difference between Samples A and B was included in the latter calculations, such that P 5 (M 1 1)/(N 1 1), where M is the number of bootstrap differences (abso- lute values) greater than or equal to the observed difference, N is the total number of bootstrap differences, and one is added to M and N to include the observed difference.

Note that this test is two tailed. Although the questions of interest are (1) whether M. leucophaeus exceeds P. pygmaeus and G. gorilla in molar size dimorphism and (2) whether L. lufengensis exceeds all of the extant comparative species in molar size dimorphism, specifying a directional alternative to the statistical null hypothesis Fig. 1. An example of the procedure used to derive P-values of no difference in sexual dimorphism requires a priori for pairwise differences among the extant species and L. lufen- justiﬁcation (i.e., evidence independent of the sample gensis. The top image shows the distribution of pairwise differ- estimates of molar dimorphism; see also Scott and ences obtained from bootstrapping two samples. The observed Stroik, 2006). For example, if it were known that post- difference between the ISDs of the two samples is 0.06; accord- cranial size dimorphism in L. lufengensis is greater than ingly, the distribution is centered on 0.06. In the bottom image, in any extant primate, then one could reasonably the bootstrap distribution has been recentered on zero. The hypothesize that other aspects of the Lufeng hominoid observed difference (0.06), represented by the vertical line, does are also extremely dimorphic, thus justifying a one-tailed not fall within the zero-centered distribution. Thus, the P-value test. for this comparison is P 5 0.0005 (i.e., 1/2001; see text for further details). This resampling procedure differs from previous appli- cations of the bootstrap (e.g., Lockwood et al., 1996, 2000; Lockwood, 1999; Silverman et al., 2001; Reno et

combined with an M2 ISD calculated using 40 males al., 2003; Villmoare, 2005; Harmon, 2006; Schrein, 2006; and 40 females, and these were combined with an M3 Gordon et al., 2008; see also Cope and Lacy, 1992) in two ISD calculated using 34 males and 34 females (see important ways. First, the latter studies are generally Table 1). concerned with determining the probability of obtaining 3. Steps 1 and 2 were performed for Sample B (e.g., from the comparative samples a sample with character- L. lufengensis), with each bootstrap sample containing istics (e.g., size, variation, sexual dimorphism) identical the same number of males and females as in Sample B. to that of a fossil sample. In the present case, however, 4. The bootstrapped ISDs for Sample A were then ran- because we are dealing with a fossil assemblage (the domly paired with those for Sample B, and the differ- sexed Lufeng specimens) that is large in comparison to ence between the ISDs for each pairing was calcu- other such assemblages, we are able to use the bootstrap lated, creating a distribution of 2000 ISD differences. to generate confidence intervals for the fossil ISD, allow- ing us to make inferences about population parameters. The middle 95% of this distribution represents the 95% Thus, we are able to incorporate the uncertainty in the confidence interval for the pairwise comparison. sample ISDs for the comparative taxa and for the fossil A pairwise difference with a 95% confidence interval species, resulting in more robust statistical testing than that does not overlap zero (i.e., no difference) can be con- is typically the case for small fossil samples (see also sidered statistically significant at the a 5 0.05 level. Gordon et al., 2008). However, we obtained more precise P-values in the fol- The second notable difference between our resampling lowing way: procedure and those used in previous studies of variation in fossil samples is that the bootstrap samples obtained 1. First, we recentered the distribution of pairwise dif- from the comparative taxa were not reduced to match ferences between Sample A and Sample B on zero the size of the fossil sample. In most of the studies cited (see Fig. 1), as outlined by Manly (1997, p 99–100). above, the statistic for the fossil sample (e.g., coefficient This step was necessary because the distribution of of variation, the index of sexual dimorphism) is used as pairwise differences will be centered on the observed a point estimate for comparison with distributions gener- difference between Sample A and Sample B. In order ated from the comparative samples. Such distributions to derive a P-value for the observed difference are composed of bootstrap samples that are identical in between Samples A and B, the distribution must be size to the fossil sample. When only a point estimate is recentered on (i.e., the mean of the distribution must used for the fossil sample, it is necessary for the samples equal) zero. According to Manly (1997, p 99), ‘‘the produced from resampling the comparative samples to idea with this approach is to use bootstrapping to ap- be the same size as the fossil sample because confidence proximate the distribution of a suitable test statistic intervals for the fossil sample are not generated. In con- when the null hypothesis is true’’ (i.e., no difference trast, because we resampled the comparative samples between samples). and the L. lufengensis sample—and thus generated con- 2. Next, using the recentered distribution, we counted fidence intervals for all of the samples—matching the the number of values that were as extreme as or sample size of the fossil sample was unnecessary and more extreme than the observed ISD difference

American Journal of Physical Anthropology MODELING SEXUAL DIMORPHISM IN MIOCENE APES 257

TABLE 2. The Sivapithecus and Ouranopithecus samples c Sex Tooth size a b Taxon Specimen assignment CP3 M1 M2 M3 Ouranopithecus RPl-55 Male** 11.7 11.6 14.2 15.9 17.8 RPl-56 Male 10.9 11.3 14.6 15.6 16.6 RPl-75 Male** 12.7 11.6 15.3 16.7 17.4 RPl-76 Male 13.2d – – – 18.1 RPl-89* Male 13.0 11.7 14.5 16.0 18.0 NKT-21 Female 8.5 9.8 11.6 13.6 13.8 RPl-54 Female** 8.5 10.1 12.3 13.6 14.2 RPl-79* Female 9 10.1 12.2 14.1 14.5 RPl-84* Female – 9.6 11.6 13.7 14.1 RPl-88* Female 8.8 9.5 12.8 14.0 14.3 Sivapithecus GSI D. 197 Male – – 11.7 14.5 – YPM 13828 Male – – 12.6 14.6 14.9 ONGC/v/790 Male – – 13.0 – – PUA 1052-69 Male – – – – 13.9 GSI 18039 Male – – 14.9 GSI 18042 Male – – 11.3 – – GSI D. 199 Female – – – 11.5 12.0 YPM 13806 Female – – – 10.6 9.9 YPM 13825 Female – – 10.1 11.3 – GSI 18041 Female – – 10.7 – – GSI 18067 Female – – – – 10.3 PUA 760-69 Female – – 9.6 – – a Data for Ouranopithecus were taken from Koufos (1993) and Koufos and de Bonis (2004); specimens marked with an asterisk (*) were not included in Schrein’s (2006) analysis. The Sivapi- thecus data were compiled by JK from various sources. b For Ouranopithecus, sex assignment is based on canine and Fig. 2. Bivariate plots of canine size vs. M2 size (top) and P3 P size (see also Fig. 2); specimens marked with double aster- 3 size vs. M2 size (bottom) in Ouranopithecus macedoniensis. isks (**) were sexed by Koufos (1995) using canine shape. For Tooth size is the geometric mean of the MD and BL dimensions. Sivapithecus, sex assignment is based on molar size (see text Specimens that were sexed based on canine shape by Koufos for further discussion). (1995) are indicated by male (#) and female ($) symbols. Note c Tooth size was calculated as the square root of the product of that (1) large and small canines and P3s cluster with the male MD and BL diameters. and female specimens, respectively, and (2) specimens with d Only the MD dimension [maximum length, identified by Kou- large molars are associated with large (male) canines and P3s, fos (1993) as ‘‘transverse diameter’’] is available for this canine. whereas specimens with small molars are associated with small (female) canines and P3s. The first and third molars exhibit a similar pattern. would have actually reduced the power of the test to detect differences, making it overly conservative. After establishing the rank order of molar dimorphism then the cluster of large specimens must be composed of in the extant species and L. lufengensis, we evaluated males and the cluster of small specimens must be com- apparent dimorphism in the Ouranopithecus macedo- posed of females (Kelley, 2005). In contrast, the distribu- niensis and Haritalyangar Sivapithecus samples. The O. tion of Haritalyangar M1s is continuous, making sex macedoniensis data used for this study were taken from assignment more arbitrary. Based on associations with the literature (Koufos, 1993; Koufos and de Bonis, 2004), M2s, three of the seven M1s can be tentatively allocated while the Sivapithecus data were provided by JK. All of to ‘‘male’’ and ‘‘female’’ clusters, while the largest the O. macedoniensis specimens used here can be confi- (ONGC/v/790) and smallest (PUA 760-69) M1s can also dently sexed based on associations with canines and P3s be assigned to the ‘‘male’’ and ‘‘female’’ groupings, (Table 2; Fig. 2; see also Schrein, 2006). This sample respectively. Two teeth—GSI 18041 and GSI 18042—fall includes newly published specimens from Ravin de la in the middle of the M1 size range. If no overlap between Pluie (Koufos and de Bonis, 2004) that were not used in males and females is assumed, then the index of ap- the most recent analysis of variation and sexual dimor- parent sexual dimorphism (ISDA) is between 1.19 and phism in this fossil ape (Schrein, 2006), and that expand 1.21, depending on whether both specimens are assigned the sample from n 5 5–6 sexed individuals per molar to one sex or if the larger GSI 18042 is grouped with position to n 5 9–10, including the addition of three presumed males and the smaller GSI 18041 is grouped complete female molar rows (for a total of five) and one with presumed females. If females and males do overlap complete male molar row (for a total of four) (Table 2). in size (with the smaller GSI 18041 placed with pre- The sample of Sivapithecus mandibular molars from sumed males and the larger GSI 18042 placed with pre- Haritalyangar is smaller, with n 5 5–7 individuals per sumed females), then the ISDA would be 1.16. We exam- molar position (Table 2), and none of these specimens ined the effect of these alternative assignments and can be sexed based on associations with canines or P3s. found that they did not substantively influence the However, the M2 and M3 samples are each characterized results. Thus, we report only the results of the analyses by the presence of two markedly disjunct size clusters. If in which GSI 18042 was considered male and GSI 18041 the Haritalyangar assemblage samples a single species, was considered female. Note that these sex assignments

American Journal of Physical Anthropology 258 J.E. SCOTT ET AL. are identical to those that would have been obtained had no difference was considered falsified at the a 5 0.05 we simply used the mean method [i.e., dividing the sam- level. For these tests, two-tailed P-values were obtained ple into ‘‘males’’ and ‘‘females’’ about the mean (Plavcan, by counting the total number of bootstrap ISD values 1994; Gordon et al., 2008)]. that were as extreme as or more extreme than the Siva- The Sivapithecus and O. macedoniensis samples were pithecus and O. macedoniensis values (including the val- evaluated using resampling methods, but because these ues for the two fossil samples) and dividing that number samples are small (n 10 for all molar positions), they by the total number of ISDs (i.e., 1001). In this case, were treated as point estimates for the purpose of com- ‘‘extreme’’ refers to values that when subtracted from paring them to the extant taxa and L. lufengensis. Fol- the comparative sample’s ISD produce a difference lowing previous studies (e.g., Lockwood et al., 1996, (regardless of sign) as large as or larger than the differ- 2000; Lockwood, 1999; Silverman et al., 2001; Reno ence produced by subtracting the fossil sample’s ISDA et al., 2003; Villmoare, 2005; Harmon, 2006; Schrein, from the comparative sample’s ISD. 2006), we bootstrapped the comparative species Because our division of the Sivapithecus sample into sexes (including L. lufengensis) to obtain samples that were was based solely on size, we also analyzed this sample using identical to the Sivapithecus and O. macedoniensis sam- a sex-blind statistic—the CV—to estimate dimorphism. For ples in size and sex ratio, creating distributions for each molar position, we bootstrapped the comparative sam- determining the probability of obtaining a sample from ples 1000 times each at a sample size equal to the Sivapithe- G. gorilla, P. pygmaeus, M. leucophaeus, and L. lufengen- cus sample but without regard to sex (i.e., the sex ratios of sis with the same level of molar dimorphism observed in the bootstrapped samples did not necessarily match the the Sivapithecus and O. macedoniensis samples. hypothesized sex ratio of the Sivapithecus sample) and cal- In the procedure describe above, resampling without culated the CV for each. For this part of the analysis, the replacement can be used instead of bootstrapping (e.g., comparative samples (including the Lufeng sample) were Gordon et al., 2008). In fact, resampling without replace- modified so that the sex ratios for each tooth were balanced ment is more likely to produce lower P-values than prior to being bootstrapped. We then compared the CVs for resampling with replacement given that, at small sample the Sivapithecus molars to the resulting distributions and sizes (e.g., n 5 5–7 in the case of the Sivapithecus analy- determined the statistical significance of the sample differ- sis), the latter can, in principle, produce samples com- ences as described above. For this analysis, we only exam- posed only of multiple entries of the largest male and ined the individual molar positions, as there are currently smallest female, or samples composed only of multiple no methods for dealing with missing data in the calculation entries of the smallest male and largest female. Clearly, of the CV. The results of these analyses did not differ sub- such samples would produce wider bootstrap distribu- stantively from the analyses in which the specimens were tions (i.e., with very high and very low ISDs) that will sexed, and thus only the ISD-based results are reported. be more likely to encompass the fossil value. However, Finally, it is important to note that, because our com- Cope and Lacy (1992, p. 361), in their study of the use of parative samples are not composed entirely of complete the coefficient of variation (CV) for evaluating variation molar rows, the P-values reported for the analyses of in fossil samples, noted that a comparative sample ‘‘of multivariate molar dimorphism should be considered ap- hundreds or thousands is needed to properly simulate proximate. For example, consider a case in which the CV sample distributions.’’ This problem motivated them molars of a species are identical in their degree of dimor- to develop a method in which a very large (n 5 10,000) phism. If a sample of 40 males and 40 females is col- simulated ‘‘population’’ is generated using descriptive lected in which the ten largest males are missing their statistics from samples of extant species. This simulated M3s, then the estimate of dimorphism for the M3 will be population is then resampled without replacement at a lower than in the other teeth. When the teeth are com- sample size equal to the fossil assemblage in order to bined and multivariate molar dimorphism is estimated, determine the probability of sampling the CV observed the estimate will be biased due to the missing M3 data. in the fossil sample from the simulated population. As Such a sample will produce a bootstrap distribution that an alternative for overcoming the intractable problem of is shifted to the left (i.e., toward monomorphism), result- limited comparative material, Lockwood et al. (1996) ing in an artificially low P-value—and a potential type II used the bootstrap to generate samples equal in size to error—in a pairwise comparison with a fossil sample. fossil samples directly from the comparative samples. In However, this problem is unlikely to be an issue in our this study, we preferred the bootstrap over resampling analysis because the missing teeth in our samples are without replacement because it is not clear that our com- not size-biased. Thus, the effects of missing data on the parative samples are sufficiently large. P-values for the analysis of multivariate molar dimor- For each molar position, two sets of 1000 bootstrap phism are likely to be minimal. Therefore, in order to samples were drawn from each of the extant species use samples that are as large as possible, we have cho- samples and from the Lufengpithecus sample, with one sen not to limit the comparative samples to only those set matching the composition of the Sivapithecus sample individuals that preserve complete molar rows. and the other matching the composition of the O. mace- 3 doniensis sample. For example, in the Sivapithecus RESULTS analysis, each bootstrap sample contained seven M1s (four males, three females), six M2s (three males, three The ISDs for the extant taxa and L. lufengensis are females), and five M3s (two males, three females). For presented in Table 3. For multivariate molar size, sam- each bootstrap sample, log-transformed (base e) ISDs ple dimorphism is greatest in L. lufengensis, followed were calculated as described above. The Sivapithecus in rank order by M. leucophaeus, P. pygmaeus, and and O. macedoniensis ISDAs (log-transformed) were then G. gorilla. This pattern is repeated at each individual compared to the bootstrap distributions; if the values for molar position with one exception: M3 sample dimor- these two fossil samples fell outside the middle 95% of phism is greater in G. gorilla than in P. pygmaeus. The the bootstrap distributions, then the null hypothesis of bootstrap tests for multivariate molar size dimorphism

American Journal of Physical Anthropology MODELING SEXUAL DIMORPHISM IN MIOCENE APES 259

TABLE 3. Indices of sexual dimorphism for the extant taxa and L. lufengensis a MALL M1 M2 M3 G. gorilla 1.08 1.06 1.07 1.11 P. pygmaeus 1.10 1.09 1.11 1.09 M. leucophaeus 1.13 1.12 1.14 1.15 L. lufengensis 1.19 1.18 1.19 1.19 a The abbreviation ‘‘MALL’’ refers to multivariate molar size here and in subsequent tables.

TABLE 4. Results of the bootstrap tests for interspeciﬁc differences in multivariate molar size dimorphism Gorilla Pongo Mandrillus Pongo 5 (0.1119) Mandrillus M [ G (0.0005) M [ P (0.004) Lufengpithecus L [ G (0.0005) L [ P (0.0005) L [ M (0.001)

Nonsignificant differences are indicated by an equality symbol; greater-than symbols indicate significance and the direction of difference. P-values for each comparison are given in parentheses (probabilities are two-tailed). Abbreviations: G, Gorilla; P, Pongo; M, Mandrillus; L, Lufengpithecus. reveal that G. gorilla and P. pygmaeus are not significantly different, whereas M. leucophaeus is significantly more dimorphic than the two extant apes, and L. lufengensis is significantly more dimorphic than all of the living species (Table 4, Fig. 3). When dimorphism is examined by molar position (Table 5), P. pygmaeus and G. gorilla differ statistically Fig. 3. Bootstrap distributions for multivariate molar size dimorphism for the extant species and L. lufengensis. The mid- only at M2, with P. pygmaeus being more dimorphic at this position. Mandrillus leucophaeus is significantly dle 95% of each distribution is equivalent to the 95% confidence more dimorphic than G. gorilla at M and M —but not interval for multivariate molar size dimorphism. Gorilla gorilla 1 2 and P. pygmaeus are not significantly different, M. leucophaeus at M3—and is significantly different from P. pygmaeus is more dimorphic than the living apes, and L. lufengensis is only at M3. Lufengpithecus lufengensis is significantly more dimorphic than all of the extant taxa. more dimorphic than the living apes at all molar positions, but is significantly more dimorphic than M. leuco- dimensions indicate that if this assemblage samples a phaeus only at M1 and M2. Some of these differences are nonsignificant after adjusting a-levels for multiple com- single species, then the distal molars of that species are parisons using the sequential Bonferroni method (e.g., even more dimorphic than those of L. lufengensis. This Rice, 1989); the results that remain significant are: M. is true for multivariate molar dimorphism as well. leucophaeus more dimorphic than G. gorilla for M1 and M2, L. lufengensis more dimorphic than the living great DISCUSSION apes for all molar positions, and L. lufengensis more dimorphic than M. leucophaeus for M1. Application of Identifying levels of sexual dimorphism in fossil spe- the sequential Bonferroni adjustment to the comparisons cies that are extreme in comparison to living species of multivariate molar size dimorphism does not alter the requires knowledge of the limits of dimorphism in extant results. taxa. In the case of L. lufengensis, previous studies have The results for the analysis of the O. macedoniensis used extant Pongo to represent the upper limit of molar sample are given in Table 6. For multivariate molar size, dimorphism in living primates (Kelley and Xu, 1991; O. macedoniensis is more dimorphic than all of the Kelley, 1993: Kelley and Plavcan, 1998). However, the extant taxa, but it is not significantly different from L. results of this study demonstrate that the molars of lufengensis (Fig. 4A). The results for M1 and M3 are sim- P. pygmaeus are not the most size-dimorphic among ilar to those for multivariate molar size, but for M2, O. extant primates; in fact, our samples do not allow us to macedoniensis is only significantly more dimorphic than unequivocally establish that P. pygmaeus is even the G. gorilla. Sequential Bonferroni adjustment renders most dimorphic living hominoid in this respect. Mandril- only the latter difference nonsignificant. lus leucophaeus emerges as the most dimorphic extant In contrast to the O. macedoniensis sample, apparent primate when the molar row is considered in its entirety, dimorphism in the Sivapithecus assemblage is signifi- but the drill cannot be consistently distinguished statis- cantly greater than in any of the comparative taxa, tically from either P. pygmaeus or G. gorilla at individ- including L. lufengensis, even after sequential Bonfer- ual molar positions (though sample dimorphism is roni adjustment (Table 7, Fig. 4B). The only exception is always greatest in the drill among the extant taxa). apparent dimorphism in the M1 sample, which cannot be While the general lack of statistical differences between statistically distinguished from M1 dimorphism in G. gorilla and P. pygmaeus in this study challenges the L. lufengensis. Thus, the Haritalyangar M2 and M3 conventional assumption that the molars of the orangu-

American Journal of Physical Anthropology 260 J.E. SCOTT ET AL. tan are more dimorphic than those of the gorilla, Uchida (1996a) documented intrageneric variation in molar dimorphism in both Pongo and Gorilla. Thus, a more (0.0885) complete analysis that includes material from eastern 5 lowland gorillas, mountain gorillas, and Sumatran orangutans could reveal differences between these two genera. It is also important to point out that our ability to detect differences among the living taxa is hampered in 3 (0.001) * (0.0305) P M

P some respects. First, ratios such as the ISD generally [

[ have wider conﬁdence intervals than the variables from L M which they are derived due to the fact that there is mea- surement error in both the numerator (male mean) and denominator (female mean) (see discussion in Smith, -values for each comparison are given

P 1999). Second, because males and females constitute sep-

(0.0005) arate components of the ISD, the effective sample sizes (0.1149) (0.4448) G for each species are about half the total sample sizes. 5 5 [ Thus, given that the differences in molar sample ISDs L among G. gorilla, P. pygmaeus, and M. leucophaeus are relatively small, especially when compared to differences in canine, craniofacial, and body-mass dimorphism across the Anthropoidea (Plavcan, 2001), it is not sur- prising that many of the comparisons in this study are * (0.0195) . An asterisk (*) indicates that the comparison is not signiﬁcant

M nonsigniﬁcant. Future studies will require larger sam-

[ ples to establish whether the differences in sample ISDs

L observed between G. gorilla and P. pygmaeus and between P. pygmaeus and M. leucophaeus at individual molar positions reﬂect true population differences. In spite of the conservative nature of the statistical 2 Lufengpithecus (0.0005) , tests, our results conﬁrm that the molars of L. lufengensis M L (0.2214) P

; are more dimorphic than those of living apes. Our analy- 5 [ sis of the Lufeng hominoid also demonstrates that it was L more dimorphic than M. leucophaeus (at least with respect to the molar row in its entirety and M1, and probably M as well). That we were able to detect signiﬁcant

Mandrillus 2

, differences between L. lufengensis and the extant species M

(0.0005) 5 ;

(0.0005) despite the fact that the Lufeng sample contains only n * (0.0325) G G G 16–22 individuals per molar position highlights just how [ [ [ much greater dimorphism is in the molar teeth of this fos- Pongo L M P , sil ape. Notably, the analysis of multivariate molar size P

; dimorphism indicates that M. leucophaeus is intermediate between the great apes and L. lufengensis (see Fig. 3). Thus, although molar dimorphism in L. lufengensis is Gorilla (0.012) , extreme relative to living primates, comparison to the G M drill reveals that it is not as extreme as it appears to be [ when only extant great apes are considered. L Despite the drill’s higher level of overall molar dimorphism compared to extant apes, its inclusion in our analysis of the O. macedoniensis material does not alter previous conclusions that a single-species interpretation of 1 (0.0005)

M this fossil assemblage necessitates a level of dimorphism (0.1339) P TABLE 5. Results of the bootstrap tests for interspeciﬁc differences at individual molar positions that exceeds that observed in living primates (Schrein, 5 [

L 2006). Although the addition of the more recent Ravin de la Pluie specimens (Koufos and de Bonis, 2004) results in slightly lower indices of apparent sexual dimorphism (ISDAs) for O. macedoniensis in comparison to those for the smaller sample used by Schrein (2006), (0.0015) (0.0005) G

(0.1009) there is still no overlap in size between specimens identi- G Gorilla Pongo Mandrillus Gorilla Pongo Mandrillus Gorilla Pongo Mandrillus [ 5 fied as male and those identified as female on the basis [ of canine or P3 size/morphology (see Table 2, Fig. 2), an attribute also evident in the L. lufengensis sample (Kelley and Plavcan, 1998). In our analysis, M2 is the only O. macedoniensis variable for which size dimorphism cannot be statistically distinguished from that of any of the extant species, except for G. gorilla prior to sequential Bonferroni adjustment. Schrein (2006) after sequential Bonferroni adjustment (applied within each variable). in parentheses (probabilities are two-tailed). Abbreviations: Nonsignificant differences are indicated by an equality symbol; greater-than symbols indicate significance and the direction of difference. Lufengpithecus L Mandrillus M Pongo obtained somewhat different results for her comparisons

American Journal of Physical Anthropology MODELING SEXUAL DIMORPHISM IN MIOCENE APES 261

TABLE 6. Bootstrap results for the Ouranopithecus comparisons Ouranopithecus

MALL (ISD 5 1.20) M1 (ISD 5 1.21) M2 (ISD 5 1.16) M3 (ISD 5 1.24) Gorilla O [ G (0.001) O [ G (0.002) O [ G* (0.018) O [ G (0.004) Pongo O [ P (0.001) O [ P (0.002) 5 (0.1339) O [ P (0.001) Mandrillus O [ M (0.001) O [ M (0.006) 5 (0.4336) O [ M (0.004) Lufengpithecus 5 (0.3407) 5 (0.3996) 5 (0.2987) 5 (0.0939)

between O. macedoniensis and the great apes (i.e., only the M1 of Ouranopithecus could be confidently identified as being more dimorphic than in gorillas and orangutans), which is probably attributable to the smaller sample of O. macedoniensis used in her study and the fact that the compositions of the Gorilla and Pongo samples were different from those used in the present analysis. Note also that Schrein (2006) examined MD and BL dimensions separately, whereas we combined them [i.e., (MD 3 BL)1/2]. Nevertheless, the pattern of results in the two studies is broadly similar. Under the assumption that fossil species could not have been more dimorphic than extant species, our results could be interpreted as supporting the presence of multiple species in the O. macedoniensis sample (e.g., Kay, 1982a). However, the fact that molar size dimorphism in O. macedoniensis cannot be statistically distinguished from that in L. lufengensis demonstrates that the level of dimorphism required for O. macedoniensis under a single-species taxonomy is not unprecedented among late Miocene hominoids. Thus, the inclusion of L. lufengensis in the comparative framework demonstrates that, although O. macedoniensis does not fit expectations regarding sexual dimorphism among extant taxa, it can be accommodated within known models of intraspecific variation and sexual dimorphism when other fossil species are used as analogues. Schrein (2006) reviewed several lines of evidence pointing to the exis- tence of only a single species within the O. macedoniensis dental sample: large specimens are male, small specimens are female; the Ravin de la Pluie specimens, which constitute the bulk of the sample, are from individuals that were sympatric and probably synchronic; and molar morphology is homogeneous. The results presented here strengthen the case for recognizing a single species among the hominoid remains from Ravin de la Pluie, Fig. 4. Bootstrap distributions for multivariate molar size Xirochori, and Nikiti, one characterized by an extreme dimorphism generated by bootstrapping the extant taxa at a sample size and sex ratio identical to that of the (A) Ouranopi- degree of molar dimorphism relative to living primates. thecus and (B) Sivapithecus samples. Only the M. leucophaeus The results of the Sivapithecus analysis, on the other and L. lufengensis distributions are shown; the G. gorilla and hand, do not lend themselves to easy interpretation. Kel- P. pygmaeus distributions would be to the left of the Mandrillus ley (2005) found that measures of variation for the distribution. The solid vertical line in A indicates the ISDA for Haritalyangar M2s and M3s are statistically significantly the O. macedoniensis sample; the dashed vertical line in B indi- higher than those for L. lufengensis, suggesting an even cates the ISDA for the Sivapithecus sample. greater level of sexual dimorphism than that exhibited by L. lufengensis if these specimens represent a single species. Our results confirm that the level of apparent Lufeng distribution, and Kelley’s (2005) analysis of vari- dimorphism in the Haritalyangar M2 and M3 samples is ation in the Haritalyangar maxillary molars indicates highly unlikely to have come from a species as dimorphic that the same would certainly be true for M1,M2, and as L. lufengensis; none of the samples bootstrapped from M3, as levels of apparent dimorphism in these teeth are the Lufeng sample produced ISDs as high as the ISDAs slightly lower than or similar to those of L. lufengensis 2 3 for the Haritalyangar M2,M3, or multivariate molar (M ISDA 5 1.16; M ISDA 5 1.19; an ISDA cannot be 1 size. In contrast, the ISDA for M1 falls well within the calculated for M due to the fact that the specimens

American Journal of Physical Anthropology 262 J.E. SCOTT ET AL.

TABLE 7. Bootstrap results for the Sivapithecus comparisons Sivapithecus

MALL (ISDA 5 1.29) M1 (ISDA 5 1.20) M2 (ISDA 5 1.32) M3 (ISDA 5 1.34) Gorilla S [ G (0.001) S [ G (0.001) S [ G (0.001) S [ G (0.003) Pongo S [ P (0.001) S [ P (0.004) S [ P (0.001) S [ P (0.001) Mandrillus S [ M (0.001) S [ M (0.01) S [ M (0.001) S [ M (0.001) Lufengpithecus S [ L (0.001) 5 (0.6533) S [ L (0.001) S [ L (0.001)

Nonsignificant differences are indicated by an equality symbol; greater-than symbols indicate significance and the direction of difference. P-values for each comparison are given in parentheses (probabilities are two-tailed). Abbreviations: G, Gorilla; P, Pongo; M, Mandrillus; L, Lufengpithecus; S, Sivapithecus. form a fairly tight cluster, precluding the use of size as a unknown. Thus, based on the current evidence, the tax- criterion for sex assignment; see Fig. 8.3 in Kelley, onomy of the Haritalyangar Sivapithecus material 2005). remains ambiguous (see also Kelley, 2005). If we accept that fossil species are not constrained by currently known limits of intraspecific variation and sex- CONCLUSIONS ual dimorphism (Kelley, 1993; Kelley and Plavcan, 1998; Plavcan and Cope, 2001; Schrein, 2006), then the single- Our analysis of sexual dimorphism in molar size in species hypothesis cannot be definitively ruled out for great apes and the drill demonstrates that the latter spe- the Haritalyangar sample, despite the fact that such a cies exceeds the extant hominoids in some aspects of species would have to be even more dimorphic than molar dimorphism. Thus, Pongo does not possess the L. lufengensis. While the high levels of size variation most dimorphic molars among living primates, though and apparent sexual dimorphism in the Haritalyangar they are among the most dimorphic. These results indi- second and third mandibular molars can be used to cate that Mandrillus leucophaeus (and perhaps other argue for the presence of two species (Kelley, 2005), such papionins) should be included in extant comparative evidence cannot be used as the sole basis for rejecting samples when evaluating variation in fossil hominoid the single-species hypothesis (Kelley and Plavcan, 1998; assemblages, particularly when variation appears to Plavcan and Cope, 2001; Schrein, 2006). Presumably, exceed that in gorillas and orangutans. We confirmed there is a limit to the amount of molar dimorphism that the extreme degree of molar dimorphism in the Lufeng- can be expressed in primates, but whether or not pithecus lufengensis sample relative to extant species, L. lufengensis (and O. macedoniensis) represents that thereby establishing the importance of using this species limit is currently unknown. Other recently reported cases as a comparative analogue to represent levels of intra- of extreme dimorphism, including the middle Miocene specific variation and sexual dimorphism not sampled hominoid Griphopithecus alpani from Pasalar, Turkey among living primates (e.g., Kelley, 2005). [apparent even though a second species has been identi- Using the drill and L. lufengensis samples as part of fied in the Pasalar assemblage (Humphrey and Andrews, our comparative framework, we analyzed apparent size 2008; Kelley et al., 2008)], and the Oligocene early catar- dimorphism in the molars of two other late Miocene rhine Aegyptopithecus zeuxis from the Fayum, Egypt hominoid assemblages that have been identified as possi- (Simons et al., 2007), could provide insight into this issue. bly comprising single highly dimorphic species. Our On the other hand, given that the Haritalyangar sec- results for the Haritalyangar Sivapithecus sample show ond and third mandibular molars do not fit any of our that, if only one species is present at this site, then it is comparative models of sexual dimorphism, additional more dimorphic than L. lufengensis for at least some lines of evidence are required before accepting a single- teeth. Given the uncertainties concerning the sex of the species taxonomy for this sample, as the two-species tax- individuals in this sample, and because the sample as a onomy cannot be rejected based on current evidence whole does not fit any of our comparative models, we are either. In this context, demonstration that the size clus- unable to choose with confidence between the hypotheses ters evident in the M2 and M3 samples are truly homoge- that the sample contains (1) a single, extremely size- neous with respect to sex using canine and/or P3 size dimorphic species or (2) two species, differing primarily and morphology, as was done for the L. lufengensis and in size. On the other hand, in the case of Ouranopithecus O. macedoniensis samples (Kelley and Xu, 1991; Kelley, macedoniensis, our analysis shows that the level of 1993; Schrein, 2006; see Fig. 2), would provide support molar dimorphism required under a single-species taxon- for the single-species hypothesis. Conversely, a two-spe- omy is fully compatible with the degree of sexual dimor- cies hypothesis—with each size cluster representing a phism in the molars of L. lufengensis, thus demonstrat- different species—would be supported if it is shown that ing that, while a single-species taxonomy for the O. mac- males and females are present in both clusters. Unfortu- edoniensis sample requires a degree of molar nately, the current sex assignments are based on size dimorphism that is extreme compared to that in living because there are no associated canines or P3s, which anthropoids, it is not extreme in comparison to at least precludes unequivocally linking the high levels of varia- one other hominoid species from the late Miocene of tion in the sample to sex differences. Eurasia. Finally, it is important to note that the temporal span for Sivapithecus at Haritalyangar, at approximately 400,000 years (Pillans et al., 2005), is certainly greater ACKNOWLEDGMENTS than for either the Lufengpithecus or Ouranopithecus samples, but how much of this range is represented in We thank Xu Qinghua of the Institute of Vertebrate the portion of the Haritalyangar sample analyzed here is Paleontology and Paleoanthropology, Beijing, China, for

American Journal of Physical Anthropology MODELING SEXUAL DIMORPHISM IN MIOCENE APES 263 providing access to the Lufengpithecus dental data while 54:455–479. sponsored by grants from the National Academy of Sci- Kelley J, Etler D. 1989. Hominoid dental variability and species ences and the Leakey Foundation to JK. We are grateful number at the late Miocene site of Lufeng, China. Am J Pri- to Michael Plavcan for answering questions regarding matol 18:15–34. his Mandrillus leucophaeus data, and Stephen Frost Kelley J, Plavcan JM. 1998. A simulation test of hominoid species number at Lufeng, China: implications for the use of the coeffi- kindly allowed us to examine Mandrillus sphinx data cient of variation in paleotaxonomy. J Hum Evol 35:577–596. that he, Rachel Nuger, and Michelle Singleton collected. Koufos GD. 1993. Mandible of Ouranopithecus macedoniensis Dennis Young provided invaluable statistical advice. (Hominidae, Primates) from a new late Miocene locality of This manuscript benefitted from thoughtful comments Macedonia (Greece). Am J Phys Anthropol 91:225–234. and suggestions by Editor-in-Chief Christopher Ruff, the Koufos GD. 1995. The first female maxilla of the hominoid Our- associate editor, and two anonymous reviewers. The anopithecus macedoniensis from the late Miocene of Macedo- bootstrap tests were performed using Microsoft Excel nia, Greece. J Hum Evol 29:385–399. macros written by Charles Lockwood—friend, mentor, Koufos GD, de Bonis L. 2004. New material of Ouranopithecus and colleague. He is missed. macedoniensis from late Miocene of Macedonia (Greece) and study of its dental attrition. Geobios 39:223–243. Kramer A. 1993. Human taxonomic diversity in the Pleistocene: does Homo erectus represent multiple hominid species? Am J LITERATURE CITED Phys Anthropol 91:161–171. Lieberman DE, Pilbeam DR, Wood BA. 1988. A probabilistic Albrecht GH, Miller JMA. 1993. Geographic variation in pri- approach to the problem of sexual dimorphism in Homo mates: a review with implications for interpreting fossils. In: habilis: a comparison of KNM-ER 1470 and KNM-ER 1813. J Kimbel WH, Martin LB, editors. Species, species concepts, Hum Evol 17:503–511. and primate evolution. New York: Plenum. p 123–161. Lockwood CA. 1999. Sexual dimorphism in the face of Baab KL. 2008. The taxonomic implications of cranial shape Australopithecus africanus. Am J Phys Anthropol 108:97– variation in Homo erectus. J Hum Evol 54:827–847. 127. Bunce M, Worthy TH, Ford T, Hoppit W, Willerslev E, Drum- Lockwood CA, Kimbel WH, Johanson DC. 2000. Temporal mond A, Cooper A. 2003. Extreme reversed sexual size dimor- trends and metric variation in the mandibles and dentition of phism in the extinct New Zealand moa Dinornis. Nature Australopithecus afarensis. J Hum Evol 39:23–55. 425:172–175. Lockwood CA, Richmond BG, Jungers WL, Kimbel WH. 1996. Cope DA. 1993. Measures of dental variation as indicators of Randomization procedures and sexual dimorphism in Austral- multiple taxa in samples of sympatric Cercopithecus species. opithecus afarensis. J Hum Evol 31:537–548. In: Kimbel WH, Martin LB, editors. Species, species concepts, Mahler P. 1973. Metric variation in the pongid dentition. PhD and primate evolution. New York: Plenum. p 211–237. dissertation, University of Michigan, Ann Arbor. Cope DA, Lacy MG. 1992. Falsification of a single species hy- Manly BFJ. 1997. Randomization, bootstrap and Monte Carlo pothesis using the coefficient of variation: a simulation methods in evolutionary biology, 2nd ed. London: Chapman & approach. Am J Phys Anthropol 89:359–378. Hall. Gordon AD, Green DJ, Richmond BG. 2008. Strong postcranial Martin L. 1991. Teeth, sex and species. Nature 352:111–112. size dimorphism in Australopithecus afarensis: results from Martin LB, Andrews P. 1993. Species recognition in middle Mio- two new resampling methods for multivariate data sets with cene hominoids. In: Kimbel WH, Martin LB, editors. Species, missing data. Am J Phys Anthropol 135:311–328. species concepts, and primate evolution. New York: Plenum. Harmon EH. 2006. Size and shape variation in Australopithecus p 393–427. afarensis proximal femora. J Hum Evol 51:217–227. Pillans B, Williams M, Cameron D, Patnaik R, Hogarth J, Sahni Harvati K, Frost SR, McNulty KP. 2004. Neanderthal taxonomy A, Sharma JC, Williams F, Bernor RL. 2005. Revised correla- reconsidered: implications of 3D primate models of intra- and tion of the Haritalyangar magnetostratigraphy, Indian Siwa- interspecific differences. Proc Natl Acad Sci USA 101:1147– liks: implications for the age of the Miocene hominids Indopi- 1152. thecus and Sivapithecus, with a note on a new hominid tooth. Humphrey LT, Andrews P. 2008. Metric variation in the postca- J Hum Evol 48:507–515. nine teeth from Pasalar. Turkey. J Hum Evol 54:503–517. Plavcan JM. 1990. Sexual dimorphism in the dentition of extant Huynen L, Millar CD, Scofield RP, Lambert DM. 2003. Nuclear anthropoid primates. PhD Dissertation, Duke University. DNA sequences detect species limits in ancient moa. Nature Plavcan JM. 1993. Catarrhine dental variability and species rec- 425:175–178. ognition in the fossil record. In: Kimbel WH, Martin LB, edi- Kay RF. 1982a. Sexual dimorphism in Ramapithecinae. Proc tors. Species, species concepts, and primate evolution. New Natl Acad Sci USA 79:209–212. York: Plenum. p 239–263. Kay RF. 1982b. Sivapithecus simonsi, a new species of Miocene Plavcan JM. 1994. Comparison of four simple methods for esti- hominoid, with comments on the phylogenetic status of the mating sexual dimorphism in fossils. Am J Phys Anthropol Ramapithecinae. Intl J Primatol 3:113–173. 94:465–476. Kelley J. 1986. Species recognition and sexual dimorphism in Plavcan JM. 2001. Sexual dimorphism in primate evolution. Proconsul and Rangwapithecus. J Hum Evol 15:461–495. Yearb Phys Anthropol 44:25–53. Kelley J. 1993. Taxonomic implications of sexual dimorphism in Plavcan JM. 2002. Taxonomic variation in the patterns of Lufengpithecus. In: Kimbel WH, Martin LB, editors. Species, craniofacial dimorphism in primates. J Hum Evol 42:579– species concepts, and primate evolution. New York: Plenum. 608. p 429–457. Plavcan JM. 2003. Scaling relationships between craniofacial Kelley J. 1995a. Sexual dimorphism in canine shape among sexual dimorphism and body mass dimorphism in primates: extant great apes. Am J Phys Anthropol 96:365–389. implications for the fossil record. Am J Phys Anthropol Kelley J. 1995b. Sex determination in Miocene catarrhine pri- 120:38–60. mates. Am J Phys Anthropol 96:391–417. Plavcan JM, Cope DA. 2001. Metric variation and species recog- Kelley J. 2005. Twenty-five years contemplating Sivapithecus nition in the fossil record. Evol Anthropol 10:204–222. taxonomy. In: Lieberman DE, Smith RJ, Kelley J, editors. Reno PL, Meindl RS, McCollum MA, Lovejoy CO. 2003. Sexual Interpreting the past: essays on human, primate, and mam- dimorphism in Australopithecus afarensis was similar to mal evolution in honor of David Pilbeam. Boston: Brill Aca- that of modern humans. Proc Natl Acad Sci USA 100:9404– demic. p 123–143. 9409. Kelley J, Andrews P, Alpagut B. 2008. A new hominoid species Rice WR. 1989. Analyzing tables of statistical tests. Evolution from the middle Miocene site of Pasalar. Turkey. J Hum Evol 43:223–225.

American Journal of Physical Anthropology 264 J.E. SCOTT ET AL.

Richmond BG, Jungers WL. 1995. Size variation and sexual Smith RJ, Jungers WL. 1997. Body mass in comparative prima- dimorphism in Australopithecus afarensis and living homi- tology. J Hum Evol 32:523–559. noids. J Hum Evol 29:229–245. Teaford MF, Walker A, Mugaisi GS. 1993. Species discrimina- Ruff CB, Walker A, Teaford MF. 1989. Body mass, sexual dimor- tion in Proconsul from Rusinga and Mfangano Islands, Kenya. phism and femoral proportions of Proconsul from Rusinga In: Kimbel WH, Martin LB, editors. Species, species concepts, and Mfangano islands, Kenya. J Hum Evol 18:515–536. and primate evolution. New York: Plenum. p 373–392. Schrein CM. 2006. Metric variation and sexual dimorphism in Uchida A. 1996a. Craniodental variation among the great apes. the dentition of Ouranopithecus macedoniensis. J Hum Evol Cambridge, MA: Peabody Museum of Archaeology and Eth- 50:460–468. nology, Harvard University. Scott JE, Lockwood CA. 2004. Patterns of crown size and shape Uchida A. 1996b. Dental variation of Proconsul from the Tin- variation in great apes and humans and species recognition deret region. Kenya. J Hum Evol 31:489–497. in the hominid fossil record. Am J Phys Anthropol 125:303– Villmoare B. 2005. Metric and non-metric randomization meth- 319. ods, geographic variation, and the single-species hypothesis Scott JE, Stroik LK. 2006. Bootstrap tests of signiﬁcance and for Asian and African Homo erectus. J Hum Evol 49:680–701. the case for humanlike skeletal-size dimorphism in Australo- Walker A, Teaford MF, Martin L, Andrews P. 1993. A new spe- pithecus afarensis. J Hum Evol 51:422–428. cies of Proconsul from the early Miocene of Rusinga/Mfangano Setchell JM, Lee PC, Wickings EJ, Dixson AF. 2001. Growth islands, Kenya. J Hum Evol 25:43–56. and ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx). Am J Phys Anthropol 115:349–360. Wood BA. 1976. The nature and basis of sexual dimorphism in Silverman N, Richmond B, Wood B. 2001. Testing the taxonomic the primate skeleton. J Zool Lond 180:15–34. integrity of Paranthropus boisei sensu strico. Am J Phys Wood BA. 1991. A palaeontological model for determining the Anthropol 115:167–178. limits of early hominid taxonomic variability. Paleontol Afr Simons EL, Seiffert ER, Ryan TM, Attia Y. 2007. A remarkable 28:71–77. female cranium of the early Oligocene anthropoid Aegyptopi- Wood BA, Xu Q. 1991. Variation in the Lufeng dental remains. thecus zeuxis. Proc Natl Acad Sci USA 21:8731–8736. J Hum Evol 20:291–311. Skinner MM, Gordon AD, Collard NJ. 2006. Mandibular size Wu R, Oxnard CE. 1983a. Ramapithecines from China: evidence and shape variation in the hominins at Dmanisi, Republic of from tooth dimensions. Nature 306:258–260. Georgia. J Hum Evol 51:36–49. Wu R, Oxnard CE. 1983b. Ramapithecus and Sivapithecus from Smith RJ. 1999. Statistics of sexual size dimorphism. J Hum China: some implications for higher primate evolution. Am J Evol 36:423–459. Primatol 5:303–344.

American Journal of Physical Anthropology