AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 134:312–322 (2007

)

Genetic, Geographic, and Environmental Correlates of Human Temporal Bone Variation
Heather F. Smith,1*y Claire E. Terhune,1*y and Charles A. Lockwood2
1 2

School of Human Evolution and Social Change, Arizona State University, Tempe, AZ 85287-2402 Department of Anthropology, University College London, London WC1E 6BT, UK KEY WORDS geometric morphometrics; molecular distance; cranial morphology were relatively high. Comparisons of morphological distances to molecular distances based on short tandem repeats (STRs) revealed a significant correlation between temporal bone shape and neutral molecular distance among Old World populations, but not when Native Americans were included. Further analyses suggested a similar pattern for morphological variation and geographic distribution. No significant correlations were found between temporal bone shape and environmental variables: temperature, annual rainfall, latitude, or altitude. Significant correlations were found between temporal bone size and both temperature and latitude, presumably reflecting Bergmann’s rule. Thus, temporal bone morphology appears to partially follow an isolation by distance model of evolution among human populations, although levels of correlation show that a substantial component of variation is unexplained by factors considered here. Am J Phys Anthropol 134:312–322, 2007. V 2007 Wiley-Liss, Inc.
C

ABSTRACT Temporal bone shape has been shown to reflect molecular phylogenetic relationships among hominoids and offers significant morphological detail for distinguishing taxa. Although it is generally accepted that temporal bone shape, like other aspects of morphology, has an underlying genetic component, the relative influence of genetic and environmental factors is unclear. To determine the impact of genetic differentiation and environmental variation on temporal bone morphology, we used threedimensional geometric morphometric techniques to evaluate temporal bone variation in 11 modern human populations. Population differences were investigated by discriminant function analysis, and the strength of the relationships between morphology, neutral molecular distance, geographic distribution, and environmental variables were assessed by matrix correlation comparisons. Significant differences were found in temporal bone shape among all populations, and classification rates using cross-validation

Like other aspects of phenotype, cranial morphology reflects a combination of genetic and environmental influences (Moss, 1962, 1972). Within this framework, some authors have suggested that particular portions of the cranium may be less prone to variation due to environmental variables, and therefore more phylogenetically informative (Olson, 1981; Strait et al., 1997; Lieberman et al., 2000a; Harvati, 2001; Wood and Lieberman, 2001; Harvati and Weaver, 2006a,b). For hominins, traits associated with heavy chewing have been argued to be homoplastic and consequently unreliable indicators of phylogeny (Walker et al., 1986; Wood, 1988; Skelton and McHenry, 1992; Turner and Wood, 1993; McHenry, 1994, 1996; Lieberman et al., 1996; but see Strait et al., 1997; Asfaw et al., 1999; Collard and Wood, 2001). The morphology of the cranial base has especially been regarded as a reliable reflection of genetic relationships, as it forms very early during ontogeny and ossifies endochondrally (Moore and Lavelle, 1974; Olson, 1981; MacPhee and Cartmill, 1986; Lieberman et al., 2000a,b). The cranial base also mirrors the shape of the developing brain, which is relatively constrained (Houghton, 1996). Basicranial characters may therefore be less influenced by epigenetic forces than are the externally sensitive intramembraneous bones of the facial skeleton. The morphology of the temporal bone, as part of the cranial base, may also reflect neutral molecular distances within species and phylogenetic relationships among species. However, the temporal bone also serves a variety of functional roles, such as posture, hearing, balance, mastication, and formation of the braincase. Consequently, this element can serve as a test case of the
C V 2007

ways in which cranial morphology covaries with molecular distances and environmental factors and a test of the hypothesis that cranial base elements have a strong genetic component. Several recent studies of variation in the temporal bone have demonstrated this region’s utility in distinguishing among species and subspecies of extant great apes, and for quantifying levels of variation within and between taxa (Harvati, 2001, 2003; Lockwood et al., 2002, 2004, 2005; Terhune et al., 2007). In particular, Lockwood et al. (2004) demonstrated that, using shape distributions of coordinate data from modern humans, orangutans, gorillas, chimpanzees, and bonobos, the resultant phylogenetic tree of these taxa was identical to the molecular phylogeny of these species. Similarly, sev-

Grant sponsors: AMNH Collections Study Grant and ASU Department of Anthropology; Grant number: NSF BCS-9982022. *Correspondence to: Heather F. Smith or Claire E. Terhune, School of Human Evolution and Social Change, Arizona State University, Box 872402, Tempe, AZ 85287-2402, USA. E-mail: heather.f.smith@asu.edu or claire.terhune@asu.edu
y

These authors contributed equally to this work.

Received 12 December 2006; accepted 8 May 2007 DOI 10.1002/ajpa.20671 Published online 13 July 2007 in Wiley InterScience (www.interscience.wiley.com).

WILEY-LISS, INC.

2001. Given this background. eral recent studies (Harvati. and waypoints (squares). Are modern human populations significantly different in temporal bone morphology? Q2. Roseman. Franciscus and Long. 2004).. 1981. Data on 783 STRs in matched analogues of nine of the human populations discussed earlier were used to obtain American Journal of Physical Anthropology—DOI 10. Terhune et al.TEMPORAL BONE VARIATION IN MODERN HUMANS 313 Fig. suggesting that other factors also play a significant role in patterns of temporal bone morphology in humans. Linear dimensions of the skull have been shown to reflect genetic relationships of human populations.. 1991. In general. and facial skeleton – with molecular distances and environmental variables. 22 landmarks from the ectocranial surface of the temporal bone were employed. we sought to investigate the association between temporal bone morphology and molecular distance among human populations. 2001. together with geographic distance and external factors such as environmental variables. Harvati and Weaver (2006a) used 13 landmarks. We also include additional environmental variables such as rainfall and altitude. The correlation between temporal bone shape and molecular distance was significant but low. 2001. Some recent studies have explicitly evaluated these influences on cranial anatomy (Relethford. These three-dimensional data were then analyzed using Morphologika (O’Higgins and Jones. Table 2). Gonzales-Jose et al. mastoid. First. (2007). Goodall. 2007) have used the morphology of the temporal bone to test hypothesized taxonomic divisions among fossil taxa. Output from these analyses (Procrustes residuals from the GPA and PC scores from the PCA) was recorded and copied into other statistical programs for further analysis. 1975. Individuals with extensive antemortem tooth loss were generally avoided to minimize the possibility of alveolar resorption affecting the morphology of the temporomandibular joint (TMJ). 2002. Harvati and Weaver (2006a. cranial vault. They concluded that the morphology of the temporal bone and cranial vault are correlated with molecular distance in human populations. Table 1).b) analyzed the correlation between human morphological variation in three cranial regions – the temporal bone. 1998). 2003. 2004. 1943). variation in shape was investigated through principal components analysis (PCA). Diversifying regional selection due to climate also affects the cranial morphology of several other human populations (Carey and Steegmann. In addition. tympanic. What is the strength of the correlation between temporal bone morphology and molecular distance among populations of modern humans? Q3. 1. while facial morphology covaries more reliably with environment. Map of the world showing the approximate locations of populations used in the morphological analysis (triangles). 2002. 1994. populations used in the molecular analysis (circles). 2. Lines link the morphological populations and their genetic representatives.1002/ajpa . Gonzales-Jose et al. Roseman. 2004). 1. such as Siberia (Roseman. 1998). Specimens were housed at the American Museum of Natural History and Arizona State University. and explore the relationship between morphology and geographic distance. However. Subsequently. Our goal is to use an independent dataset and an expanded set of landmarks on the temporal bone to replicate part of the study of Harvati and Weaver (2006a). such that closely related populations tend to be more similar in overall cranial form (Relethford. temporal bone centroid size was found to be correlated with temperature. we are testing the hypothesis that the temporal bone follows an isolation by distance model of evo- lution in human populations (Wright. selective pressures acting on the skull of certain human populations have also been identified and can have a significant impact on cranial morphology of populations living in regions with extreme temperatures. Dryden and Mardia. An Immersion Microscribe point digitizer was used to record the three-dimensional coordinates of each landmark. More specifically. Following Lockwood et al. a finding that is consistent with environmental variation in body size as first outlined by Bergmann (1847). 2004. 1998. (2002). 2004). and intraobserver error for a subset of the data set used here is reported by Terhune et al. In comparison. and petrous portions of the temporal bone (Fig.. three-dimensional coordinate data were registered through a generalized Procrustes analysis (GPA) (Gower. 2004). All threedimensional data were collected by the second author. Roseman. 1991. three research questions were investigated: Q1. How do external variables such as environmental differences or geographic distance covary with patterns of temporal bone morphology in humans? MATERIALS AND METHODS Data collection A total of 243 individuals from 11 modern human populations were included in this study (Fig. which describe the morphology of the mandibular fossa.

it was necessary to substitute a representative population from the same geographic region and/or linguistic group (Table 1). 109. Twenty-two temporal bone landmarks digitized in the present study (following Lockwood et al.5E 4N.23 103. 2004. American Journal of Physical Anthropology—DOI 10. 1999.b).63 98.21 100.43 94. Roseman. 19.35 94.4N. The Alaskan natives and southern India sample had to be omitted from the molecular analysis as neither they nor any other comparable population has been typed for a sufficient number of STR loci.8E 37. (2005) and Rosenberg et al. Utah) New Guineans Nubians (Semna South.52 98. Analytical methods The first research question examined the degree to which the morphology of the temporal bone can discriminate among populations of Homo sapiens. Several of the populations measured in the craniometric study have not been typed for STRs. and the significance of these values was assessed via a permutation test (Good. However. Harvati and Weaver. The link between these environmental variables and temporal bone morphology could stem directly from local adaptations of cranial shape or indirectly from behaviors mediated by the environment. This practice has been employed in previous studies of the relationship between morphological and molecular distances in modern humans (Relethford. This form of significance testing compares the observed distance (i. neutral molecular distances. 166.314 a H. Data were also compiled on environmental variables in regions from which the populations originated. 38.5E 46. altitude.7W 34.1E 4. these populations were still included in all other analyses in this study.e. 2006a.43 102.91 97. Open circles show the relative positions of landmarks 1 and 18 when these landmarks are not directly visible.0N. 1994. 150. such as diet or activity levels. SMITH ET AL. Refer to Table 2 for landmark definitions.64 Average geographic coordinates 68. 77. 103. particularly the archaeological samples (the Nubians and Medieval Hungarians).56E Alaskan Natives Australian Aborigines Hungarians (Medieval) Khoisan Malaysians Mongolians Native American (Grand Gulch. and latitude. 1993). using data from nearby weather stations (New et al. Sudanese Nubia) Pare (Tanzania) Southern Indians Total a Specimens were housed at Arizona State University (Nubians) or the American Museum of Natural History (all others). The dataset used here was originally used by Ramachandran et al. 2002). where individuals are randomly allocated to each group and a mean distance is calculated. 2000) and almanacs. TABLE 1. 109. 30. These loci are autosomal and evolve neutrally such that shared mutations are accepted as evidence of common ancestry. an average location was used.4S. 138. Procrustes distances between groups were calculated..9N.. 18. STRs have been shown to be particularly useful and appropriate for determining genetic relationships of populations of Homo sapiens. test statistic) with a distribution of permuted distances. These included rainfall..F. Approximate geographic coordinates of population origins were estimated using an atlas and published information for the samples.6N.8W 6. In the case that a range of coordinates was obtained.5S. 2.1002/ajpa .8S. temperature. and was evaluated in two ways.4E 20. A test statistic is considered statistically significant Fig.3S.1E 13N. In these cases.69 98.69 98.2E 20. First. Modern human populations used in the morphometric analysis Population Total 20 21 21 19 21 18 20 20 43 19 21 243 Genetic representative None Australians French San Cambodians Mongolians Pima Papua New Guineans Mozabite Kenyan Bantu None Centroid size 106. (2005) and consists of the largest and most inclusive STR dataset published to date.6N.5E 46.

McNulty... 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 Definition 315 Intersection of the infratemporal crest and sphenosquamosal suture Most lateral point on the margin of foramen ovale Most anterior point on the articular surface of the articular eminence Most inferior point on entoglenoid process Most inferior point on the medial margin of the articular surface of the articular eminence Midpoint of the lateral margin of the articular surface of the articular eminence Center of the articular eminence Deepest point within the mandibular fossa Most inferior point on the postglenoid process Anteromedial apex of the petrous part of the temporal bone Most posterolateral point on the margin of the carotid canal entrance Most lateral point on the vagina of the styloid process (whether process is present or absent) Most lateral point on the margin of the stylomastoid foramen Most lateral point on the jugular fossa Center of the inferior tip of the mastoid process Most inferior point on the external acoustic porus Most inferolateral point on the tympanic element of the temporal bone Point of inflection where the braincase curves laterally into the supraglenoid gutter. molecular or environmental distances). Since the Nubian sample was significantly larger than all other samples used here (n 5 43). 2005). Athreya and Glantz. 2005.. However.05) if it is reached or exceeded in less than 5% of the random permutations. 1986) in PopTools. a discriminant function analysis (DFA) was conducted using the first 40 PC scores from the PCA of Procrustes coordinates (which accounted for [95% of variation). 2005). and a subset of 404 of the same STRs has been typed in Native Australians. morphological distances (i.1). Second. (2002). size or shape distance matrices) were compared to the variable of interest (e. 1997.0. and these two distance measures were found to be significantly correlated (r 5 0.. where prior probabilities were set equal to group size. while a number of authors ´ (Ackermann. The second research question addressed the degree of concordance between temporal bone shape and genetic relationships among human populations. P \ 0. The differentiation among populations was then assessed using discriminant analyses with jackknife cross-validation. Analogous studies above the species level have compared phylogenetic trees based on morphology with those based on molecular data (Lockwood et al. a reduced sample of 20 randomly chosen individuals was used for this analysis. This relationship was tested by examining the correlation between matrices of temporal bone morphology (i.e. a distance measure analogous to FST but specifically designed for microsatellite loci in assuming a stepwise mutation model (Slatkin. size and shape matrices) and molecular distances. Lycett and Collard. to assess the role of allometry. Smouse et al. only Procrustes distances are reported here.. Analyses using both of these distance measures were found to lead to the same general pattern of results. 2004.e. 2004. (P-value 0. 2003). For each analysis. Rosenberg et al. a size matrix (i. 2006a. Strait and Grine. The current analysis is therefore restricted to matrix correlation comparisons. 2002. 2002..b) have previously used Mahalanobis distances in analyses such as this. STR data were analyzed using Arlequin 3. 2005). Additionally. Harvati and Weaver. In contrast. 2002. Klingenberg and Monteiro. allometry) are not removed. 2003. see also Collard and Wood. an addon for Microsoft Excel. 1976..001). The degree and significance of the correlation between the distance matrices from the molecular and morpho- American Journal of Physical Anthropology—DOI 10. within humans.. Mahalanobis distances are affected by uneven sample sizes. 2005. correlations between centroid size and shape were evaluated by regressing the principal component axes on centroid size using Morphologika..TEMPORAL BONE VARIATION IN MODERN HUMANS TABLE 2. This assumption is tenuous given the sample sizes used here. differences in covariance structure between populations should not affect these distances as drastically as they would affect Mahalanobis distances. Although Procrustes superimposition scales all specimens to the same unit centroid size.e.1002/ajpa .. A matrix of STR population distances was constructed using Slatkin’s genetic distance. Also. 2005. DFAs were conducted using SPSS (version 11. as Mahalanobis distances attempt to account for within group variation by scaling the values by a pooled within-group covariance matrix. 2005). Both Procrustes and Mahalanobis distances were calculated for all populations used here. size related shape changes (i. Data on 783 STRs have been typed for eight representative populations (Ramachandran et al. since Procrustes distances are not scaled by the pooled within-group covariance matrix.g. However. in coronal plane of the mandibular fossa Point on lateral margin of the zygomatic process of the temporal bone in the coronal plane of the postglenoid process Auriculare Porion Asterion After Lockwood et al. 1995). a tree-like structure does not apply to population relationships for morphological or molecular information (summarized by Sherry and Batzer. Definitions of landmarks used in the present study No.. Therefore. which assumes that all groups in the analysis have similar covariance structures (Ackermann. 2004. 2001. Harvati. Strand Viðarsdottir et al.0 (Excoffier et al..662. a matrix of the absolute differences in centroid size between groups) was calculated and compared with the Procrustes distance (or shape) matrix using a Mantel test (Mantel.e. Harvati et al. while no similar bias has been noted for Procrustes distances.

Russia. The inclusion of waypoints.390 0.131 0.186 20.064 0.069 20.11 1. TABLE 3.028 20.196 0.029 0. did not usually traverse large bodies of water (Ramachandran et al. RESULTS In the DFA.051 0.029 20. again in PopTools.037 5 0.068 20. As expected.93 0.18 8.327 0.055 0.173 0.091 0.130 20.019 20.44 1.00 Canonical correlation 0. The hypothesis that temporal bone morphology covaries with geographic distance was then assessed by comparing the geographic matrix with the morphological matrix using a Mantel test.136 0.035 0.211 0. rainfall.039 0.006 20. To address the possibility that environmental factors influenced morphological difference.21 0.030 0. rather than a line of minimal geographic distance that could run across an ocean.064 PC1 PC2 PC3 PC4 PC5 PC6 PC7 PC8 PC9 PC10 PC11 PC12 PC13 PC14 PC15 PC16 PC17 PC18 PC19 PC20 0. Canada.316 0.012 0.046 0.142 0.211 20.031 20.124 0.033 0. Cairo.56 0.010 0.057 20.060 0.056 0.242 20.141 0. permits a more accurate estimate of the migrational distance among populations. the morphological distance matrices were compared to each environmental matrix using a Mantel test. A single overall environmental distance matrix (Euclidean distance. the expected proportion of correct random classifications is 9%.005 0.225 0.286 0.69 2.140 0. latitude.070 0.037 20.015 20.085 20.50 0. so these results indicate high success rates.165 0.224 0. Following Ramachandran et al. Ramachandran et al. Environmental distance matrices were generated for each environmental variable: temperature.110 0.149 0.81 58. the first function is influenced by a variety of principal components and accounts for just over 40% of variance among populations (Tables 3 and 4). therefore.087 20.58 0.127 0. SMITH ET AL.052 20. All correlations are reported as Pearson product moment correlation coefficients (r).1002/ajpa .05. waypoints included were Anadyr.122 20.066 20.113 0.133 0.77 0.084 0.379 0.75 0.062 20.149 0.068 20.150 6 20.070 0.74 5.018 4 20.063 0.244 0. For 11 populations of roughly equal sample size.061 0. 1).230 20.149 0.005 0.056 20.91 0.125 0.316 H. and Prince Rupert.165 20.018 0.094 0.61 0.250 20.009 0.200 0.037 0. Permutation tests of the Procrustes distances among populations were all statistically significant with P-values of less than 0.81 17.223 20. and altitude. contributions of subsequent functions diminish rapidly (Table 4).034 20.001 0.135 20.034 20.011 0.012 0.175 0.076 20.144 20.025 0.080 0.97 83. Eigenvalues.049 0.013 0.033 20.053 0. and canonical correlations for the discriminant function analysis Function 1 2 3 4 5 6 7 8 9 10 Eigenvalue 6.096 0. Structure matrix for the discriminant function analysis (first 20 PCs only) showing the correlations between each of the PC axes and discriminant functions Function 1 2 0.092 0. A geographic matrix was generated using great circle distances and including five waypoints (Fig.065 0.28 % of variance 40.140 0. alpha was set at 0.053 0.74 0. Phnom Penh.015 0.82 3. plus any distances between waypoints if more than one waypoint fell between the populations. Finally.33 0.80 Cumulative % 40.050 20.015 7 0. Egypt.102 0.105 0.246 0.038 0.010 20. this factor is considered later in discussing the results.169 20. environmental variables and geographic distances for populations were evaluated to determine how they covary with temporal bone morphology.071 0.53 93.71 89.45 0.010 0. This practice takes into account the conclusion that most human migrations.22 96.238 20.152 0.208 0.093 0.037 20.070 0.022 20.059 20.78 1.051 20. It is probable even within TABLE 4.043 20.037 0.203 20.072 0.196 20. 2004.037 0.023 0.073 3 20.164 20.193 0.138 20.079 0.098 20. The pairwise distance between any two populations was calculated as the sum of the distance between Population 1 and the waypoint.029 0.206 20.073 0. Great circle distances use latitude and longitude and take into account the fact that these coordinates are on the circumference of a sphere to calculate distances between two locations.445 0.189 20.001 (Table 5).F.023 20.287 20.39 2.09 98.042 0.137 0.061 0. with classification rates between 56 and 85% (mean 73%) (Table 6).044 0.020 20.123 20.124 20.023 0. until recently. geographic great circle distances among populations were calculated..071 20.060 20. and between the waypoint and Population 2.105 0. incorporating data from all four environmental variables) was also calculated in PopTools.028 20.129 10 20.56 67.. American Journal of Physical Anthropology—DOI 10.093 0.127 0.018 0.210 20.182 0.022 20.094 0.043 0.381 20.192 0.032 0.276 9 0.086 8 0.062 20. 2005).049 logical analyses was assessed using a Mantel test. Istanbul.69 0.29 1.113 20.228 0.118 0.86 0.47 continents that migrational distances are affected by geographical barriers and are not simply great circle distances.309 0.014 20.156 20.142 20.164 20.035 0. Turkey.145 20.75 9. geographic locations through which populations would have had to travel when migrating between two continents (Relethford. To test the association between geography and morphology.049 20.033 0.052 0. Cambodia.133 0.143 20.037 20.439 0. 2005). distribution of variance.153 0.23 7. For all analyses.022 20.081 20.74 75.102 20. Geographic distances among populations on the same continent were calculated as normal great circle distances.172 0.141 0.87 2.069 0.121 20.094 0.312 20.088 0.357 20. The DFA with crossvalidation demonstrates that the populations can be distinguished relatively well. (2005).20 100.182 20.

0848 – 0.0707 0.0719 0.0525 0.0799 0.0551 0.0958 0.0798 0.0788 0.0715 0.0681 0.0853 0.0603 0.0744 0. with a priori probabilities based on group sample sizes.0574 0.0476 0. Each horizontal row summarizes the number of correct classifications for each group as well as misclassifications. 1 Nubian was misclassified as a Native American.0634 0.089 – 0.1100 0.0546 0.g.0727 0.075 0.0667 0.0704 0.0828 – 0.0804 0.0562 0.0709 0.0953 0.0669 0.0628 Native Americans Nubians Native Americans Australians Alaskans Hungarians Pare Malaysians Khoisan New Guineans Mongolians Indians – 0.0797 – 0.0740 0.0904 0..1002/ajpa Jackknife cross-validation is the ‘‘leave-one-out’’ method as implemented in SPSS.0643 0.0633 0.0821 – 0.0783 – 0. Procrustes distances between groups Australians Alaskans Hungarians Pare Malaysians Khoisan New Guineans Mongolians Indians Nubians – 0.0677 – 0.0793 0.0689 0.0835 0.TABLE 5.0664 – 0.0947 0.0699 0.0656 0. Classification results of the discriminant function analysis using jackknife cross-validation Native Americans 1 16 1 1 2 1 0 0 0 0 0 0 0 16 1 2 1 2 0 1 4 0 0 0 0 17 0 0 2 1 0 0 0 2 1 1 0 15 0 2 0 0 0 0 Australians Alaskans Hungarians Pare 1 0 1 0 0 13 0 0 0 0 0 Malaysians 0 1 1 1 0 1 15 0 1 0 0 Khoisan 0 0 0 0 1 2 0 14 0 0 0 Mongolians 0 0 0 0 0 0 0 1 10 0 1 New Guineans 0 0 1 0 0 0 0 1 2 13 3 Indians 0 0 0 0 0 0 0 2 4 3 17 TEMPORAL BONE VARIATION IN MODERN HUMANS % Correct Nubians Nubians Native Americans Australians Alaskans Hungarians Africans Malaysians Khoisan Mongolians New Guineans Indians 80 80 76 85 71 68 71 74 56 65 81 16 2 0 0 1 1 0 0 0 0 0 American Journal of Physical Anthropology—DOI 10.0703 – TABLE 6. e.0559 0.0763 0.0721 0. 317 .074 0.059 0.0792 0.0707 0.0745 0.

geographic.05.948 7.001 0.677 4.218 3. P 5 0. Results for the comparison of morphological and molecular distance are substantially different depending on whether the Utah Native American sample is included.829 8. R2 \ 0.032.056 0.713a 20.784 Molecular distance Molecular without Utah Native Americans Geography Geography without Utah Native Americans Temperature Rainfall Latitude Altitude Combined environment 0.11 0.523 2. When it is included along with all other populations.15).021 0.129 20.712 3. In explaining this result. where R2 5 0.740 4.629.337 1. in some cases.003 0. shape: r 5 0.293 r 0.516 0.003).736 8.029 0.208 0. neutral genetic distances are not distributed in a way that facilitates comparison to morphological distances in this group. geographic. No significant correlation was found between the temporal bone shape matrix and any of the environmental matrices.998 11.106 P 0.046 – 1. rainfall.205 0.792 0.199 8.912 2.261 – 11.175 0. the analysis excluding Native Americans is probably more representative of the true pattern of relationships.221 0.694 5. the molecular distance between the Native American group and others was an order of magnitude greater than distances observed between other populations. regression of the first 30 principal components (which account for 90% of the sample variance) on centroid size indicated that.05 20.175 4.990 – 8.298.215 4.537 0.298 20.541 3. Pairwise differences in centroid size among all populations used in the morphometric analysis – 5.179 0. size: r 5 0.28).04).318 Indians – H.143 0. although the centroid size and molecular distance matrices remained uncorrelated (r 5 20. Mantel tests for morphological. Excluding the Native American sample. and environmental matrices Shape Mongolians r – 8.00001).794 3. Results of the Mantel tests performed between morphological matrices (shape and size) and the molecular.480 1. TABLE 8. with the exception of PC 4.521 4. There was also no significant correlation between the size matrix and the environmental variables of altitude. These results suggest that while there may be some allometric affects within the sample as a whole.15 0.523 8.157 0. the correlation between molecular distances (Table 9) and temporal bone morphology was not statistically significant (molecular distance vs.218 3. P 5 0.233 0.875 0. Additionally. we note that the molecular distances between the Native Americans and all other populations were extremely high (Table 9).872 Khoisan – 0. although a number of these PCs are significantly correlated with size.695 5.e.911 2.074 6. molecular distance vs.216 8.738 4.144 20. a Correlations significant at P \ 0. P 5 0.389 0.271 3. the R2 values for these correlation are very low (i.1002/ajpa Calculated as the absolute difference in centroid size.032 0.469).172 and the P-value was highly statistically significant (P \ 0.593 0.114 0.741 0. Results of this analysis indicate that the size and shape matrices are uncorrelated (r 5 20.200 5. At least according to the STR data.419 0.420a 20.043 – 7.499 0. morphological differentiation between populations is not primarily a result of allometry.205.175.666 5.119 4. molecular. Size matrix Nubians Native Americans Australians Alaskans Hungarians Pare . Allometric affects within the sample were assessed using a Mantel test of the correlation between the Procrustes distance shape matrix (Table 5) and the size matrix (Table 7).123. P 5 0.004 3. See Table 1 for the mean centroid sizes for each population.584 Nubians Native Americans Australians Alaskans Hungarians Pare Malaysians Khoisan New Guineans Mongolians Indians – 4. SMITH ET AL.095 0.018 2. P 5 0.103 Size P 0.566 r 5 Pearson correlation coefficients.415 0.782 – 0.075 3.837 5. Therefore. the correlation between the Procrustes distance and molecular distance was strongly significant (r 5 0. or the combined environmental Malaysians – 2.045 20.338a 20.629a 0.282 1.552 2.. and environmental differences are summarized in Table 8.709 American Journal of Physical Anthropology—DOI 10.425 1.327 New Guineans TABLE 7.F.028 20.469 0.195 0.

1993. Lockwood et al. and size and latitude (r 5 0. P 5 0. and the nature of the environmental influence on this element is unclear.001). Harvati et al. P 5 0. 1999. The correlation between geographic distance (Table 10) and morphological distance for all 11 populations was not significant (geography vs. Gonzales-Jose et al. Santos et al.06230 – 0. 2001. although the correlation with centroid size dropped to r 5 0.09888 – 0.07021 – These values were calculated using Slatkin’s genetic distance for microsatellites (Slatkin. who found a significant correlation between molecular and morphological distances using different populations and different temporal bone landmarks from this study. While neutral molecular markers may drift unchecked. 2002.420.07. However. This finding may indicate that the modern genetic analogue.06320 0. Monsalve et al.15853 0.021). and the results suggest that: 1) there are significant differences in temporal bone morphology among modern human populations. 2003.. while their morphology is broadly similar to other groups. as indicated in bold.095. 2007). Our goal was therefore to explore the relationship between temporal bone morphology and genetic. Roseman.05739 – 0.07179 0.. it remained significant (P 5 0. 2) shape (but not size) differences partially reflect neutral evolution.20845 0. was not representative of the older morphological sample from Grand Gulch.029). the marked genetic differentiation of the Pima sample may be the result of the extreme bottle-necking hypothesized to have occurred during the migration of early Americans to the New World (Szathmary. The finding that the morphology of the temporal bone reflects genetic relationships among human populations is consistent with studies that have identified an association between other aspects of cranial morphology and genetic relationships in humans (Relethford. size: r 5 0. Since Harvati and Weaver (2006b) found that the correlation between size and climate was only obtained if their specifically cold-adapted population was included in the analysis. altitude. For latitude. 2004. 2004). and it may therefore serve as a reliable means of assessing relationships when molecular data are unavailable.09976 0.713.03417 – 0.338. Battilana et al. P 5 0.01).15405 0. our results without Native American samples are similar to those of Harvati and Weaver (2006a. or whether it is primarily a single cold-adapted population driving the correlation. and it provides an important comparison for previous analyses that have used the temporal bone to discriminate between species and subspecies of great apes and fossil hominins (Harvati.TEMPORAL BONE VARIATION IN MODERN HUMANS TABLE 9. Overall. as it does among hominoid species. However.12706 0. Utah. matrix.11).233.07665 0.03697 0. Temporal bone morphology. a significant positive correlation was found between size and temperature (r 5 0.. geography vs. the Alaskan population was removed from the comparisons of size to temperature and latitude. These results are also consistent with those of Harvati and Weaver (2006a. Three hypotheses were tested. The rationale for removing this population is to determine whether there is a general pattern of correlation among all populations. Lockwood et al..07455 0.09838 Australians French Kenyan Bantu Cambodians San New Guineans 319 Mongolians – 0..001). Alternatively.. 2006).11348 0.11735 0.15705 0. or temperature. 2004.01643 0.13097 0.1002/ajpa ..00487 – 0.05328 0. Note the high values of molecular distances between the Native American population (Pima) and all other populations. The STRs used in this study were found to show a significant correlation with geographic distances (r 5 0. 2004. Lockwood et al.05266 0. in addition to the difficulty in explaining low morphological distances between Native Americans and other groups. removal of the Utah Native American population increased the correlation substantially. P \ 0.10778 0.07951 0.08725 0. The temporal bone contains information about genetic relationships within humans. 2002. the degree to which it reflects neutral genetic evolution has not been fully addressed..04371 Pima – 0.04064 0. 3) geographic distance is a significant factor but plays a smaller role in shape variation. A bottle-neck event may explain why the molecular distance of the Native Americans is high relative to other populations and perhaps exaggerated.b). Although it initially appeared that the correlation between molecular distance and morphological distance based on the temporal bone was not significant.05873 0.569. 4) shape of the temporal bone is not significantly associated with climate.. and genetic differentiation Our analysis shows that the temporal bone has high discriminatory power for human populations even when analyzed on its own. who also did not include a native North American sample in their genetic analysis. P 5 0. 2002. 2004).779.07234 0. the correlation with size dropped to a nonsignificant correlation of r 5 0. Bortolini et al. This result is consistent with similar studies on humans and other taxa (Harvati. 2003.08941 0. Molecular distance matrix Mozabite Mozabite Pima Australians French Kenyan Bantu Cambodians San New Guineans Mongolians – 0. and geographic variation. However removal of the Utah Native American group from the analysis resulted in a significant correlation between geographic distance and morphology (r 5 0.05430 0. environmental. and 5) size of the temporal bone is significantly correlated with temperature and latitude. DISCUSSION Although the shape of the temporal bone has long been used in analyses of population affinities and species relationships. 1995). In any case.b).03332 0. For temperature. the Pima. the cranium is likely to be under some degree of stabilizing selection.221.06628 0. P 5 0. shape: r 5 0. the molecular distance matrix among Old World populations American Journal of Physical Anthropology—DOI 10. group affiliation. Terhune et al.04588 0. the correlation between molecular and morphological distance of the temporal bone was relatively good. 1995..

838 9. and specifically to food material properties and dental function (Bouvier. Together with the genetic correlation. some aspects of TMJ shape have been linked to variation in masticatory function.260 4. this finding indicates that the temporal bone is evolving to some degree under an ‘‘isolation by distance’’ model (Wright.629 2. Mongolians Geographic distance There is also a general association between morphological and geographic distances.452 8. These environmental variables are not entirely separate entities. neutral genetic distance..347 – 4.922 15.855. other factors play a substantial role in temporal bone morphology in humans.139 10.780 1.320 Indians Distances were calculated using great circle distances including five waypoints through which populations would travel during migrations.612 14.384 10.4432 5. Alaskans Australians Native Americans Nubians American Journal of Physical Anthropology—DOI 10.F.989 13. Thus.699 17.913 5. explains only 39% of morphological variation in the temporal bone.735 – 19.496 Environment None of the environmental variables included in this study (altitude.486 9.236 17. 1999. The relationship of geographic distance. or temperature (they did not look at rainfall).126 10. it seems likely that temperature is the predominant environmental influence over human temporal bone size.244 13.001).121 – 9.610 10.662 4. there may be a threshold beyond which additional geographic distance does not translate into additional morphological distance.038 Pare – 14. the Utah Native American group may share morphology with distant populations due to aspects of ecology not studied here.558 10. which predicts that variation increases with geographic distance among populations. latitude. See Figure 1 and Table 1 for approximate locations of populations. Harvati and Weaver (2006a.326 4. New Guineans Khoisan TABLE 10.963 14.925 17. who found that temporal bone shape was not significantly associated with humidity.871 13.1002/ajpa Nubians Native Americans Australians Alaskans Hungarians Pare Malaysians Khoisan New Guineans Mongolians Indians – 14. 1943.976 19. Also. 1986a.883 – 9. These findings are consistent with those of Harvati and Weaver (2006a.050 . rainfall.206 15.942 3. Temporal bone size. P \ 0. Vinyard et al.935 9. was found to covary with temperature and latitude.673 – 12.758 3. and temporal bone morphology points to the neutral component of temporal bone variation.836 6. the correlation between morphological and geographic distance was only significant if the Utah Native American population was removed from the analysis. As one might expect. Some of this variation may be related to variation in the shape of the cranial component of the TMJ.837 – 18. – H. Although temporal bone shape correlates with genetic and geographic distance between populations. Wall. latitude.462 6.226 9. As with the molecular distance analysis.118 9.686 14. 1971. CavalliSforza et al..984 12.474 4.952 7. SMITH ET AL. the morphology of which is described by the landmarks included in this study.978 5.632 2. Morton et al.281 9.b) also found temporal bone size to be correlated with temperature. largely because of the inclusion of a sample from Alaska. the size of the temporal bone is probably less informative than temporal bone shape for inferring genetic affinities between populations. Along similar lines.830 6. as the temperature and latitude matrices were found to be highly correlated with each other (r 5 0. 1847). 1994). as would be predicted by Bergmann’s Rule (Bergmann.834 18.104 – 15. and that the correlation with latitude is simply a by-product of that effect.276 19. a relatively large proportion of human temporal bone variation remains unexplained by the factors investigated here..b. and temperature) showed a significant correlation with temporal bone shape.650 13. however.b). Clearly. This pattern may reflect the recent arrival of humans into the Americas. Within primates. but its morphological distances to other groups were not particularly high. This group had the highest average geographic distance from all other populations. especially if stabilizing selection restricts the potential variation in temporal bone morphology.815 2. Geographic distances between populations (in kilometers) Malaysians Hungarians – 6.

our conclusions are tempered by the absence of significant correlations with geographic distance when a native North American samples is included. Mardia KV. Am J Phys Anthropol 122:134–146. Gottinger Stud 3:595–708. Psychometrika 40:33–50. Dryden IL. Proc R Soc Lond B Biol Sci 53:285–340. dissertation.TEMPORAL BONE VARIATION IN MODERN HUMANS 2003). These results confirm the findings of Harvati and Weaver (2006a. ¨ ¨ Bergmann C. Hurtado AM. Syst Biol 54:678–688. Further analysis should focus directly on diet in an effort to partition the effects of different environmental factors and to obtain more direct indicators of the environmental component of human temporal bone shape. 2005. This manuscript was greatly improved by comments from Mark Spencer. Bedoya G.b) and are consistent with the use of temporal bone shape to study population affinities. Am J Phys Anthropol 69:473– 482. Menozzi P. Proc Natl Acad Sci USA 101:1147– 1152. 1996. Generalised procrustes analysis. and classification rates (cross-validated) are relatively high for the 11 populations studied here. and by unusually high molecular distances from this population to other human groups. In: Harrison T. Human nasal protrusion. LITERATURE CITED Ackermann RR. Homoplasy and the early hominid masticatory system: inferences from analyses of extant hominoids and papionins. Although significant. Human cranial anatomy and the differential preservation of population history and climate signatures. Australopithecus garhi: a new species of hominid from Ethiopia. Am J Phys Anthropol 85:419–427. Biomechanical scaling of mandibular dimensions in New World monkeys. Neanderthal taxonomy reconsidered: implications of 3D primate models of intra. 2002. this study shows the potential information available when morphological details of skull shape are quantified. Bouvier M. Harvati K. J Hum Evol 48:643–646. Piazza A. Weaver TD. Arlequin ver. Harvati K. 2006. Krylov M. Lieberman DE. the material properties of foods utilized by the populations sampled in this study may be a significant factor in the observed morphological variation. Cavalli-Sforza LL. 1975. Gower JC. Am J Phys Anthropol 123:69–77. latitude. Freitas LB. editors.D. Wood B. 321 CONCLUSIONS Based on geometric morphometric analysis and DFA. Dordrecht: Springer. Salzano FM. 2003. Carey JW. latitude. Gonzales-Perez E. Ph. Lovejoy O. 1847. Batzer MA. and altitude). However. New York: Cambridge University Press. Simpson S. Variation in human nasal height and breadth. Patterns of phenotypic covariation and correlation in modern humans as viewed from morphological integration. Ravosa MJ. Yrbk Phys Anthropol 43:117–169. Good P. 3. Ann Hum Genet 66:255–259. Goldani A. Bonatto SL. Klingenberg CP. Weaver TD. Am J Phys Anthropol 120:323–338. Bouvier M. London: Wiley. Ackermann RR. Procrustes methods and the statistical analysis of shape (with discussion). Athreya S. Monteiro LR. Thus. Laval G. 2000a. further work. Harvati K. Excoffier L. The Neanderthal problem: 3-D geometric morphometric models of cranial shape variation within and among species. A biomechanical analysis of mandibular scaling in Old World monkeys. Neandertals revisited: new approaches and perspectives. Patterns of covariation in the hominoid craniofacial skeleton: implications for paleoanthropological models. Tsuneto LT. Munkhbat B. Bortolini MC. Y-chromosome biallelic polymorphisms and Native American population structure. Houghton P. Alu insertion polymorphisms in Native Americans and related Asian populations. Petzl-Erler ML. 2005. Int J Primatol 7:551–567. 2002. White T. Van der Molen S. temperature. Collard M. Franciscus RG. 2001. American Journal of Physical Anthropology—DOI 10. Fagundes NJ. Ann Hum Biol 33:142–160. Princeton. Layrisse Z.1002/ajpa . Temporal bone shape does not correlate strongly with the environmental variables included here (rainfall. 2003. is necessary to resolve other factors involved in temporal bone shape. 1999. 2004. The primate cranial base: ontogeny. Benevolenskaia L. Ross CF. Glantz MM. Distances and directions in multidimensional shape spaces: implications for morphometric applications. 1981. J Hum Evol 41:167–194. Deininger PL. function. Reliability of cranial morphology in reconstructing Neandertal phylogeny. Latimer B. 1998. Steegman AT. 2006a. New York: Springer-Verlag. Hill K. Suwa G. 2001. ACKNOWLEDGMENTS Special thanks go to Katerina Harvati and Timothy Weaver for sharing their book chapter with us while it was still in press. Frost SR. the present study found that modern human populations can be distinguished from one another on the basis of their temporal bone shape. The impact of character correlation and variable groupings on modern human population tree resolution. Therefore. p 239–254. 1991. The history and geography of human genes. 1991. pointing to a small but significant neutral component of temporal bone variation that may reflect an isolation by distance model of population differentiation. Gonzales-Jose R. Hernandez M. Statistical shape analysis. J Hum Evol 42:167–187. Evol Bioinform Online 1:47–50. Munkhtuvshin N. Ueber die Verhaltnisse de Warmeokonomie ¨ des Thieres zu ihrer Grosse. Heller AH. Science 284:629–635. Am J Phys Anthropol 56:313–319. Harvati K.0: an integrated software package for population genetics data analysis. and climate. Katerina Harvati. Anat Rec A 288:1225–1233. The people of the great ocean: aspects of human biology in the early Pacific. as well as the utility of this element when preserved in isolation in the fossil record. 2006b. Arnett FC. 1986a. Goodall CR. McNulty KP. The main environmental effect is seen between temporal bone size and temperature and latitude. Variation in Neandertals: a response to Harvati (2003). 1994.and interspecific differences. the editor Clark Larsen. particularly on dietary effects. Salzano FM. Permutation tests: a practical guide to resampling methods for testing hypotheses. Asfaw B. 1993. Ruiz-Linares A. Differences among populations in temporal bone shape are correlated with geographic and neutral molecular distances. Tarazona-Santos E. Battilana J. and integration. 2004. Schneider S. Although the temporal bone is only one element of the skull. and one anonymous reviewer. 2005. Long JC. Harvati K. Bau CH. We are grateful to Ian Tattersall and Gary Sawyer of the American Museum of Natural History and Diane Hawkey of Arizona State University for permission to study collections in their care. City University of New York. NJ: Princeton University Press. Quantitative analysis of Neanderthal temporal bone morphology using three-dimensional geometric morphometrics. the correlations between temporal bone shape and molecular and geographic distances also show that much of the observed variation in temporal bone morphology can be explained by other factors. Harvati K. 1986b. Castro-De-Guerra D.

Languages. and anatomy. 1998. Homoplasy and early Homo: an analysis of the evolutionary relationships of H. 2. Am J Phys Anthropol 116:13–25. A model of temporomandibular joint function in anthropoid primates based on condylar movements during mastication. Spain). 1997. Relethford JH. London: Academic Press. Wall CE. Pena SDJ. Helgason A. Proc Natl Acad Sci USA 101:12825–12829. Tempo and mode of human evolution. Cavalli-Sforza LL. Moniz MA. Am J Phys Anthropol 109:67–88. Mitochondrial DNA and ancient population growth. Detecting interregionally diversifying natural selection on modern human cranial form by using matched molecular and morphometric data.006. PLoS Genet 1:660–671. Basicranial morphology of the extant hominoids and Pliocene hominids: the new material from the Hadar Formation. Contemporary issues in human evolution. 2004.322 H. 2004. 1997. habilis sensu stricto and H. Bioassay of kinship. Martinez I. and the effect of study design on the inference of human population structure. McHenry M. In: Stringer CB. editors. Turner A. Slatkin M. Aspects of human evolution. p 99–128. 1998.jhevol. Syst Zool 35:627–632. geography and HLA haplotypes in native American and Asian populations. Modeling human evolution—to tree or not to tree. 2005. Deshpande O. Hulme M. Proc Biol Sci 266:2209–2216. Philadelphia: Lea & Febiger. 2002. 1993. J Hum Evol 24:301–318. Relethford JH. Kimbel WH. Szathmary EJE. Williams SH. Evolutionary history of the ‘‘robust’’ australopithecines. New York: Kluwer Academic/Plenum. 1988. Am J Phys Anthropol 118:393–398. Graecopithecus. Strait DS. J Hum Evol 38:291–315. Lavelle CJB. I. Craniometric variation among modern human populations. Genetics of aboriginal North Americans. Grine FE. J Anat 193:251–272. Salzano FM. The functional matrix. Devine DV. Nature 322:517–522. McHenry HM. Harris DE. 1995. Roseman CC. Hum Biol 73:629–636. doi:10. Cartmill M. Pilbeam DR. Lieberman DE. In: Meikle WE. 1972. Mantel N. Twenty years of functional cranial analysis. Lew R. II. Roseman CC. p 219–275. Moore WJ. Multiple regression and correlation extensions of the Mantel test of matrix correspondence. 2007. Comparative palaeontological context for the evolution of the early hominid masticatory system. Am J Phys Anthropol 120:153–170. 2005. Lockwood CA. Cancer Res 27:209–220. Grine FE. 2005. J Clim 12:829–856. London: Taylor and Francis. and Sivapithecus. Homoplasy. Theor Popul Biol 2:507–524. Vistas in orthodontics. Relethford JH. Lieberman DE. Wood BA. Leakey RE. Collard M. Genetics 28:114–138. 2000b. Sokal RT. Apportionment of global human genetic diversity based on craniometrics and skin color. editors. 1986. J Clim 13:2217–2238. Hutz M. 1962. Am J Orthod 61:479–485. 1996. Ethiopia and its significance in early human evolution and taxonomy. New York: Aldine de Gruyter. Coimbra CEA. In: Kraus B. rudolfensis. 2001. The temporal bones from Sima de los Huesos Middle Pleistocene site (Sierra de Atapuerca. 1999. Comparative functional analysis of skull morphology of tree-gouging primates. J Hum Evol 32:17–82. 2005. Jones N. Isolation by distance. Proc Natl Acad Sci USA 101:4356–4360. Moss ML. 2004. Santos FR. Kimbel WH. Mowbray KM. Wood BA. editors. Genetics 139:457–462. Harris JM. Wood B. 1992. Basicranial influence on overall cranial shape. O’Higgins P. J Anat 201:211–229. Relethford JH. 2000. Jones P. Lockwood CA. editor. 2007. Growth of the facial skeleton in the Hominoidea. Hum Biol 76:499– 513. Support from the rela- American Journal of Physical Anthropology—DOI 10. J Hum Evol 23:309–349. Lynch JM. clusters. Ramachandran S. Evolutionary relationships among early hominids. Lynch JM. Morphometrics and hominoid phylogeny: support for a chimpanzee–human clade and differentiation among great ape species. Lynch JM. Representing twentieth-century space-time climate variability. Evol Anthropol 1:202–220. Trans R Soc South Africa 60:73–77. Riedel R. 1974. Further evidence for the existence of a major founder Y chromosome haplotype in Amerindians. Are the ‘robust’ australopithecines a monophyletic group? In: Grine FE. 1994. clades and hominid phylogeny. Development of 1961– 90 monthly grids of terrestrial surface climate. Jablonski NG. Jones P. A geometric morphometric assessment of the hominoids supraorbital region: affinities of the Eurasian Miocene hominoids Dryopithecus. Do homoiologies impede phylogenetic analyses of the fossil hominids? An assessment based on extant papionin craniodental morphology. Global patterns of isolation by distance based on genetic and morphological data. tionships of genetic and geographic distance in human populations for a serial founding effect originating in Africa. Lycett SJ. J Hum Evol 49: 618–642. Modern morphometrics in physical anthropology. J Anat 201:447–464. 2002. Am J Phys Anthropol 105:1–7. 1999. Inferring hominoid and early hominid phylogeny using craniodental characters: the role of fossil taxa. Kimbel WH. editor. J Hum Evol 33:283–318. p 77–92. Wright S. editor. J Hum Evol 47:399–452. Skelton R. Hulme M. Craniodental variation in Paranthropus boisei: a developmental and functional perspective. Facial growth in Cercocebus torquatus: an application of three-dimensional geometric morphometric techniques to the study of morphological variation. Erwin J. Am J Phys Anthropol 95:53–62. Lieberman DE. SMITH ET AL. New M. Basicranial structures and primate systematics. J Hum Evol. 1994. 1986. Ramachandran S. McHenry HM. 1997. Clines. A geometric morphometric study of regional differences in the ontogeny of the modern human facial skeleton. Strait DS. evolution. 1943. Sherry ST. The detection of disease clustering and a generalized regression approach. 1: systematics. O’Higgins P. Vol. 1986. Global analysis of regional differences in craniometric diversity and population substructure. 1993. New York: Liss. Arsuaga JL. Pritchard JK. Vinyard CJ. Hylander WL. Batzer MA. Olson TR.1002/ajpa . San Francisco: California Academy of Sciences. Comparative primate biology.01. 2004. A reappraisal of early hominid phylogeny. 1967. Braz J Genet 18:669–672.1016/j. Development of a 1961– 90 mean monthly terrestrial climatology. Pearson OM. McNulty KP. Genome Res 7:947–949. Lockwood CA. Variation and diversity in Homo erectus: a 3-D geometric morphometric analysis of the temporal bone. Proc Natl Acad Sci USA 91:6780–6786. Mahajan S. In: Slice D. Walker A. ´ Strand Viðarsdottir U.F. 1995. New M. Smouse PE. A measure of population subdivision based on microsatellite allele frequencies. Feldman MW. Representing twentieth-century space-time climate variability. Morton NE. Relethford JH. p 85–98. MacPhee RDE. Wood BA. Variation in early hominin temporal bone morphology and its implications for species diversity. Kenya. Brown FH. 1971. A phylogenetic approach. 1999. Rosenberg NA. Quantifying temporal bone morphology of great apes and humans: an approach using geometric morphometrics. Santos RV. Feldman MW. Moss ML. p 269–284. J Hum Evol 30:97–120. Stringer C. 2003. 2002. Monsalve MV. Terhune CE. Proc Natl Acad Sci USA 102:15942–15947. Rosenberg NA. Zhao C. Kimbel WH. Wall CE. 2001. p 349–371. In: Swindler DR. 1996. 1981.5-Myr Australopithecus boisei from west of Lake Turkana. Lockwood CA. Yee S. Long JC. 2005. Howell FC.