Locomotor Anatomy and Biomechanics of the Dmanisi Hominins

Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch

Year: 2010

Locomotor anatomy and biomechanics of the Dmanisi hominins

Pontzer, H ; Rolian, C ; Rightmire, G P ; Jashashvili, T ; Ponce de León, M S ; Lordkipanidze, D ; Zollikofer, C P E

Abstract: The Dmanisi hominins inhabited a northern temperate habitat in the southern Caucasus, approximately 1.8 million years ago. This is the oldest population of hominins known outside of Africa. Understanding the set of anatomical and behavioral traits that equipped this population to exploit their seasonal habitat successfully may shed light on the selection pressures shaping early members of the genus Homo and the ecological strategies that permitted the expansion of their range outside of the African subtropics. The abundant stone tools at the site, as well as taphonomic evidence for butchery, suggest that the Dmanisi hominins were active hunters or scavengers. In this study, we examine the locomotor mechanics of the Dmanisi hind limb to test the hypothesis that the inclusion of meat in the diet is associated with an increase in walking and running economy and endurance. Using comparative data from modern humans, chimpanzees, and gorillas, as well as other fossil hominins, we show that the Dmanisi hind limb was functionally similar to modern humans, with a longitudinal plantar arch, increased limb length, and human-like ankle morphology. Other aspects of the foot, specifically metatarsal morphology and tibial torsion, are less derived and similar to earlier hominins. These results are consistent with hypotheses linking hunting and scavenging to improved walking and running performance in early Homo. Primitive retentions in the Dmanisi foot suggest that locomotor evolution continued through the early Pleistocene.

DOI: https://doi.org/10.1016/j.jhevol.2010.03.006

Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-44323 Journal Article Accepted Version

Originally published at: Pontzer, H; Rolian, C; Rightmire, G P; Jashashvili, T; Ponce de León, M S; Lordkipanidze, D; Zollikofer, C P E (2010). Locomotor anatomy and biomechanics of the Dmanisi hominins. Journal of Human Evolution, 58(6):492-504. DOI: https://doi.org/10.1016/j.jhevol.2010.03.006 Our reference: YJHEV 1441 P-authorquery-v7

AUTHOR QUERY FORM

Journal: YJHEV Please e-mail or fax your responses and any corrections to:

E-mail: [email protected]

Article Number: 1441 Fax: +31 2048 52789

Dear Author,

Any queries or remarks that have arisen during the processing of your manuscript are listed below and highlighted by ﬂags in the proof. Please check your proof carefully and mark all corrections at the appropriate place in the proof (e.g., by using on-screen annotation in the PDF ﬁle) or compile them in a separate list.

For correction or revision of any artwork, please consult http://www.elsevier.com/artworkinstructions.

Articles in Special Issues: Please ensure that the words ‘this issue’ are added (in the list and text) to any references to other articles in this Special Issue.

Uncited references: References that occur in the reference list but not in the text e please position each reference in the text or delete it from the list. Missing references: References listed below were noted in the text but are missing from the reference list e please make the list complete or remove the references from the text. Location in Query / remark article Please insert your reply or correction at the corresponding line in the proof Q1 Kindly check the afﬁliations.

Q2 Please check the hierarchy of section headings.

Q3 The following references have been changed to match the reference list: “Hermann et al., 1998” to “Hermann and Egund, 1998”“Geissman (1986)” to “Geissmann (1986)”“Harcourt-Smith and Aeillo, 2004” to “Harcourt-Smith and Aiello, 2004”. Please verify. Q4 Please check the placement of footnotes citations 1e4 have been made at the end of the sentence “Parsing the independent effects.” Please check. Q5 Kindly check the layout of the tables.

Q6 Kindly provide the signiﬁcance of italics in Table 3.

Q7 Please note that there is a mention of part ﬁgures in the caption but there is no corresponding labels provided in the ﬁgure. Please verify.

Electronic ﬁle usage Sometimes we are unable to process the electronic ﬁle of your article and/or artwork. If this is the case, we have proceeded by: , Scanning (parts of) your article , Rekeying (parts of) your article , Scanning the artwork

Thank you for your assistance. ARTICLE IN PRESS YJHEV1441_proof ■ 6 April 2010 ■ 1/13

Journal of Human Evolution xxx (2010) 1e13

Contents lists available at ScienceDirect

Journal of Human Evolution

journal homepage: www.elsevier.com/locate/jhevol

1 56 2 Locomotor anatomy and biomechanics of the Dmanisi hominins 57 3 58 4 a,* b c d,e e 59 5 Herman Pontzer , Campbell Rolian , G. Philip Rightmire , Tea Jashashvili , Christoph P.E. Zollikofer , 60 e d 6 Marcia Ponce de Leon , David Lordkipanidze 61

7 a 62 Q1 Department of Anthropology, Washington University, St Louis, MO 63130, USA 8 b Department of Cell Biology & Anatomy, University of Calgary, Calgary, T2N 4N1 Alberta, Canada 63 9 c Department of Anthropology, Harvard University, Cambridge, MA 02138, USA 64 d 10 Georgian National Museum, 0105 Tbilisi, Georgia 65 e 11 Anthropologisches Institut, Universität Zürich, 8057 Zürich, Switzerland 66 12 67 13 68 article info abstract 14 69 15 70 Article history: 16 The Dmanisi hominins inhabited a northern temperate habitat in the southern Caucasus, approximately 71 Received 18 September 2009 1.8 million years ago. This is the oldest population of hominins known outside of Africa. Understanding 17 PROOF 72 Accepted 2 March 2010 the set of anatomical and behavioral traits that equipped this population to exploit their seasonal habitat 18 successfully may shed light on the selection pressures shaping early members of the genus Homo and the 73 19 Keywords: ecological strategies that permitted the expansion of their range outside of the African subtropics. The 74 20 Dmanisi abundant stone tools at the site, as well as taphonomic evidence for butchery, suggest that the Dmanisi 75 Biomechanics 21 hominins were active hunters or scavengers. In this study, we examine the locomotor mechanics of the 76 Early Homo 22 Hominin evolution Dmanisi hind limb to test the hypothesis that the inclusion of meat in the diet is associated with an 77 23 increase in walking and running economy and endurance. Using comparative data from modern humans, 78 24 chimpanzees, and gorillas, as well as other fossil hominins, we show that the Dmanisi hind limb was 79 25 functionally similar to modern humans, with a longitudinal plantar arch, increased limb length, and 80 fi 26 human-like ankle morphology. Other aspects of the foot, speci cally metatarsal morphology and tibial 81 torsion, are less derived and similar to earlier hominins. These results are consistent with hypotheses 27 82 linking hunting and scavenging to improved walking and running performance in early Homo. Primitive 28 83 retentions in the Dmanisi foot suggest that locomotor evolution continued through the early Pleistocene. 29 Ó 2010 Published by Elsevier Ltd. 84 30 85 31 86 32 87 33 88 34 Q2 Introduction limbs, shorter pedal phalanges, and a rigid longitudinal plantar arch 89 35 (Shipman and Walker, 1989; Aiello and Dean, 1990; Bramble and 90 36 The locomotor anatomy of fossil hominins is notable for its Lieberman, 2004). Recently, we reported new post-cranial fossils 91 37 variability (Aiello and Dean, 1990; Klein, 1999; Harcourt-Smith and for hominins from the site of Dmanisi that possess a mix of prim- 92 38 Aiello, 2004; Conroy, 2005). Nonetheless, two broad grades of itive and derived features (Lordkipanidze et al., 2007). In this paper, 93 39 locomotor anatomy can be distinguished within the last 4 million we assess the locomotor mechanics and energetics of these hom- 94 40 years of hominin evolution (Klein, 1999; Bramble and Lieberman, inins and discuss the selection pressures shaping the transition 95 41 2004; Conroy, 2005). Members of the older group, the australo- from Australopithecus to Homo. 96 42 pithecines, were habitual terrestrial bipeds that retained several Many of the derived hind limb features of the genus Homo 97 43 primitive features related to arboreal locomotion, including rela- suggest improved walking and running performance relative to the 98 44 tively long arms and short hind limbs, long, curved phalanges, and australopithecines. Increased hind limb length, evident in Homo 99 45 a funnel-shaped torso with narrow shoulders and superiorly erectus and later hominins, decreases the energy cost of walking 100 46 oriented glenoid fossa (Aiello and Dean, 1990; Ward, 2002; Bramble and running in humans (Minetti et al., 1994; Steudel-Numbers and 101 47 and Lieberman, 2004; AlemsegedUNCORRECTED et al., 2006). In contrast, Tilkens, 2004; Steudel-Numbers, 2006) and other terrestrial 102 48 members of the genus Homo possess a suite of derived post-cranial animals (Kram and Taylor, 1990; Pontzer, 2005, 2007a,b; Pontzer 103 49 traits associated with greater cursoriality, including longer hind et al., 2009). The stiff longitudinal plantar arch, which may be 104 50 present as early as Homo habilis (Harcourt-Smith and Aiello, 2004), 105 51 improves efficiency in two ways: first, by acting as a spring during 106 52 * Corresponding author. running, storing energy during midstance and returning it during 107 53 E-mail address: [email protected] (H. Pontzer). toe-off (Ker et al., 1987; Alexander, 1991), and secondly, improving 108 54 109 e Ó 55 0047-2484/$ see front matter 2010 Published by Elsevier Ltd. 110 doi:10.1016/j.jhevol.2010.03.006

Please cite this article in press as: Pontzer, H., et al., Locomotor anatomy and biomechanics of the Dmanisi hominins, J Hum Evol (2010), doi:10.1016/j.jhevol.2010.03.006 ARTICLE IN PRESS YJHEV1441_proof ■ 6 April 2010 ■ 2/13

2 H. Pontzer et al. / Journal of Human Evolution xxx (2010) 1e13

111 walking economy by providing rigidity to the foot during toe-off. opportunity to test the hypothesis that the locomotor adaptations 176 112 The shorter toes of Homo decrease the digital flexor muscle work evident in early Homo are related to foraging demands, rather than 177 113 required during the second half of the stance phase (Rolian et al., climate or size-related pressures. 178 114 2009) and should, in principle, decrease the energy needed to In this paper, we examine anatomical features of the Dmanisi 179 115 swing the leg by decreasing the mass of the foot (Myers and hind limb and investigate the functional implications for locomotor 180 116 Steudel, 1985; Browning et al., 2007). Other features, such as the performance in these hominins. Using comparative data from 181 117 fully adducted and more robust first ray, larger articular surfaces in African apes, humans, and other fossil hominins, we test the 182 118 the hind limb, derived anatomy of the gluteus maximus muscle, hypothesis that the Dmanisi hominins show improved locomotor 183 119 and enlarged calcaneal tuberosity evident in Homo may also endurance and economy relative to earlier hominins. We also 184 120 improve walking and running endurance and economy (Bramble compare the Dmanisi hominins with African H. erectus and later 185 121 and Lieberman, 2004; Lieberman et al., 2006). hominins to examine the additional effects of climate and increased 186 122 The emergence of these locomotor adaptations in the early body size on locomotor anatomy. Finally, because the Dmanisi 187 123 Pleistocene has led several authors to suggest that the transition hominins are the oldest members of the genus Homo to preserve 188 124 from Australopithecus to Homo reflects a change in foraging both a complete hind limb and partial foot, we examine the 189 125 behavior and an increase in daily travel distance (Shipman and implications of their morphology for hominin locomotor evolution. 190 126 Walker, 1989; Isbell et al., 1998; Bramble and Lieberman, 2004; 191 127 Pontzer, 2006). Specifically, it has been proposed that the evolu- Materials and methods 192 128 tion of Homo in the early Pleistocene marks the advent of carnivory 193 129 and the inclusion of meat as a substantial proportion of the diet Materials 194 130 (Shipman and Walker, 1989; Bramble and Lieberman, 2004; 195 131 Pontzer, 2006). This hypothesis is supported by the advent of Post-cranial fossils from the site of Dmanisi in the Republic of 196 132 stone tools and the evidence of butchery at some early Pleistocene Georgia were reported and described previously (Lordkipanidze 197 133 sites (Klein, 1999). Comparative studies in extant mammals suggest et al., 2007). The hind limb elements include a femur (D4167), 198 134 that carnivory entails increased locomotor demands. Living, patella (D3418), tibia (D3901), talus (D4110), medial cuneiform 199 135 hunting and scavenging carnivores travel four times farther per (D4111),PROOFfirst metatarsals (D2671, D3442), third metatarsals (D2021, 200 136 day, on average, than similarly sized herbivores (Garland, 1983; D3479), fourth metatarsals (D2669, D4165), and fifth metatarsal 201 137 Carbone et al., 2005). Thus, a shift in the diet to include more (D4058). The femur, patella, tibia, talus, and three metatarsals 202 138 meat would likely necessitate increased travel and may have led to (D2021, D4165, D4058) appear to belong to one adult individual, 203 139 selection for endurance and economy. while the other material may belong to three smaller individuals 204 140 Others have proposed that alternative selection pressures (Lordkipanidze et al., 2007). All visible epiphyses are fused, 205 141 underlie the anatomical changes evident in the early Pleistocene. although material from one smaller individual (D2671, D2669) is 206 142 For example, the long limbs and slender build of early African associated with subadult humeri (Lordkipanidze et al., 2007). We 207 143 H. erectus may be an adaptation for maintaining high activity levels focus on the femur, tibia, talus, and metatarsals in this study. 208 144 in warmer climates, increasing the ratio of skin surface area to body Comparative data for chimpanzees (Pan troglodytes), gorillas 209 145 mass to promote convective heat loss and reduce heat stress, (Gorilla gorilla), and modern humans (Homo sapiens) were collected 210 146 following Allen’s rule (Ruff and Walker, 1993; Walker, 1993). at the Cleveland Museum of Natural History (HamanneTodd 211 147 Alternatively, the derived body proportions of early Pleistocene Collection), Powell-Cotton Museum, American Museum of Natural 212 148 Homo may be a pleiotropic effect of increased body size (Lovejoy, History, Peabody Museum of Archeology and Ethnology (Harvard 213 149 1999), which may have increased in response to socio-ecological University) and the Harvard University Museum of Comparative 214 150 pressures (O’Connell et al., 1999; Wrangham et al., 1999), or to Zoology. Ape material is primarily from wild-shot specimens. The 215 151 reduce mortality during childbirth associated with increased brain human material is from 20th century Americans (HamanneTodd 216 152 size (Lovejoy, 1999). Unfortunately, because warm climate, carni- Collection) and 15e16th century Eastern Europeans (Mistihalj 217 153 vory, and large body size occur together in East African sites from Collection, Peabody Museum). Sample sizes and composition 218 154 which early Homo is known, parsing the relative effects of these varied among analyses, as is discussed for each comparison. 219 155 selection pressures has not been possible in the African fossil Data for other fossil hominins were taken from the literature or 220 156 record. from casts at Washington University and Harvard University. For 221 157 Recent finds from the Georgian site of Dmanisi, dated to the the early modern human (EMH) and Neanderthal samples, body 222 158 earliest Pleistocene at 1.77 million years ago (Lordkipanidze et al., masses were taken from Ruff et al. (1997) while femur and tibia 223 159 2007), provide an important new perspective on this debate and lengths were taken from Trinkaus (1981). The Neanderthal sample 224 160 the origin of our genus. The site of Dmanisi is located in a northern consists of nine individuals (Amud 1, La Chappelle 1, La Ferrassie 2 225 161 temperate climate (41 North latitude) in a region that currently and 4, Spy 2, Shanidar 1, 5 and 6, and Tabun C1), while the EMH 226 162 maintains a climate that is approximately 17 C cooler than the sample consists of 12 (Grotto des Enfants 4 and 5, Predmosti 3, 4, 9, 227 163 Turkana basin of Kenya (see Supplementary Information), where 10 and 14, Skhul 4, 5 and 6, Caviglione 1, Baousso da Torre 1). For the 228 164 many early Pliocene specimens of African H. erectus have been KNM-WT 15,000 skeleton, a body mass of 51 kg was used, following 229 165 recovered. The fossil hominins atUNCORRECTED Dmanisi retain a number of a recent study of body mass estimation in juvenile humans (Ruff, 230 166 primitive features, including a relatively small brain (Vekua et al., 2007). 231 167 2002; Rightmire et al., 2006) and small stature (Lordkipanidze 232 168 et al., 2007), compared with penecontemporary African H. erec- Measurements 233 169 tus. This suggests the Dmanisi hominins were not under heat stress 234 170 and did not have the larger body and brain size associated with In assessing locomotor performance in the Dmanisi hominins, 235 171 African H. ergaster or H. erectus sensu lato. However, the numerous we focused primarily on skeletal traits that have been directly 236 172 manuports and stone tools found at Dmanisi, as well as evidence for linked to economy and efficiency in experimental studies. Specifi- 237 173 butchery in the form of cut marks on bovid long bones cally, we examined hind limb length, which has been shown to be 238 174 (Lordkipanidze et al., 2007), indicate some degree of carnivory in the single largest anatomical determinant of locomotor cost in 239 175 these hominins. Thus, the Dmanisi hominins provide an terrestrial animals (Pontzer, 2007a,b), and the presence of a plantar 240

H. Pontzer et al. / Journal of Human Evolution xxx (2010) 1e13 3

241 arch, which has been shown to improve the efficiency of the human axis of the distal articular surface. The projections of these 306 242 foot (Ker et al., 1987). Hind limb length was measured in relation to eminences were marked and used to calculate torsion angle by 307 243 estimated body mass and the presence of a plantar arch was subtracting 90 from the angle included by the projected axis and 308 244 assessed using the pattern of metatarsal torsion, as discussed the line of reference. For metatarsal V, the proximal articulation is 309 245 below. In addition, we examined metatarsal robusticity and tibial oblique to the major axis of bone, and thus determining torsion was 310 246 torsion to determine whether the habitual pattern of metatarsal found to be easier with the metatarsal head resting on the table. 311 247 loading in the Dmanisi hominins was similar to that of modern With the metatarsal placed head-down and the major axis of the 312 248 humans, and whether any differences in metatarsal loading regime head coincident with the reference line, the projected major axis of 313 249 might be due to differences in tibial torsion. Element dimensions the proximal articular surface was marked and the angle between 314 250 and torsion angles were measured as follows. the proximal and distal axes was determined as above. In order to 315 251 maintain consistency among rays, 90 was subtracted to give the 316 252 Linear dimensions torsion angle because the major axis of the proximal articular 317 253 Bicondylar length of the femur (M2; Martin, 1957) and surface in metatarsal V is orthogonal to those of the other meta- 318 254 maximum length of the tibia (M1a; Martin, 1957) were measured tarsals. Where distal ends are missing (i.e., in some fossil specimens) 319 255 using a custom-made osteometric board. For the Dmanisi sample, but the orientation of the shaft is clear, torsion was measured using 320 256 linear measurements of the tarsals and metatarsals were taken the major axis of the distal surface of the broken shaft (Fig. 1D). 321 257 using standard digital calipers. In the extant sample, metatarsal Our method for determining torsion is similar to the approach 322 258 linear measurements were collected from digital scans taken on used by Largey et al. (2007), although their process for determining 323 259 a flatbed scanner at a resolution of 300 dpi (MicroTek i320 Scan- the articular axes differed from that used here. Largey et al. (2007) 324 260 Maker, Carson, CA, see Rolian et al., 2009 for details). The scanner determined the proximal and distal axes based on the cross- 325 261 method has been validated in several morphometric studies (e.g., sectional properties of the metatarsal shaft, whereas here these axes 326 262 Hallgrimsson et al., 2002; Young and Hallgrimsson, 2005), and were determined as the major axes of the articular surfaces. In 327 263 provides several advantages over camera or caliper based methods, keeping with previous studies (Largey et al., 2007), medial rotation of 328 264 including reduced measurement error and parallax. Measurements the metatarsal heads (i.e., pronation) was considered positive torsion, 329 265 for comparative fossil material were taken from the literature, or, while lateralPROOF rotation (i.e., supination) was considered negative 330 266 when necessary, from casts. torsion. A small intraobserver repeatability study was done to assess 331 267 the reliability of our method. Ten metatarsals (two of each ray) were 332 268 Metatarsal torsion each measured five times using the method described above. The 333 269 Metatarsal torsion, measured about the long axis of each meta- mean standard error of measurement for each set of five repeated 334 270 tarsal, was calculated by comparing the major axis of the proximal measurements was Æ1.3, and the mean range of measurements for 335 271 and distal articular surfaces (Fig. 1C and D). The major axis was a five-measurement set was 6.9 (maximum range 12.0). For 336 272 defined as the longest diameter of the articular surface. The meta- comparison, between-group differences in metatarsal torsion for rays 337 273 tarsal was rested with its proximal end on graph paper on a hard IIeIV were typically in excess of 20 (see below). 338 274 surface with the long axis of the bone standing vertically. The major 339 275 axis of the proximal articular surface was aligned to coincide with Tibia torsion 340 276 a line of reference (i.e., a line on the graph paper). Sighting down, Torsion about the long axis of the bone (i.e., torsion in the 341 277 along the long axis of the bone, the projected endpoints of the major transverse plane) was measured using digital photographs (Can- 342 Ò 278 functional axis of the distal articular surface were then marked on on ). The tibia was set on a table, posterior surface down, with its 343 279 the graph paper. These two marks were then connected with a line, distal end near the table’s edge. A photograph of the talar articular 344 280 and the angle included between this line (the major axis of the surface was then taken, with the camera oriented in the same plane 345 281 metatarsal head) and the reference line (the major axis of the as the articular surface. This process was repeated for the proximal 346 282 proximal articular surface) was taken as the degree of metatarsal articular surface, with the tibia’s proximal end near the table edge. 347 Ò 283 torsion. The graph paper was scanned and the angle was measured These digital images were then examined in ImageJ . For the image 348 Ò 284 using ImageJ . This method was modified for the metatarsals I and V. of the distal articular surface, the midpoints of the lateral and 349 285 For metatarsal I, the sesamoid eminences on the plantar margin of medial margins of the articular surface were located and a line was 350 286 the head were found to be more reliable indicators of the functional drawn connecting these two midpoints. The angle between this 351 287 352 288 353 289 354 290 355 291 356 292 357 293 358 294 359 295 UNCORRECTED 360 296 361 297 362 298 363 299 364 300 365 301 366 302 367 303 368 Figure 1. Measuring torsion in the tibia (A and B) and in the metatarsals (C and D). For the tibia, the angle of the proximal or talar end (gray lines) is measured with reference to the 304 edge of the table. Note that the distal tibia is elevated slightly on a foam mat in B to protect the distal end. This was not done for all specimens. For the metatarsals, the major axis 369 305 lines for the proximal and distal articular ends are shown. Metatarsals shown are left MTIV D2669 (C) and right MTIII D2021 (D). 370

4 H. Pontzer et al. / Journal of Human Evolution xxx (2010) 1e13

371 line and the edge of the table was used to determine the Distal hominoids (McHenry, 1992). Linear measurements and RHL for 436 372 Articular Angle. For the image of the proximal surface, the midpoint species and specimens included in our analyses are given in Table 1. 437 373 of the anterioreposterior axis of each condylar surface was located 438 Ò 374 using ImageJ , and a line was drawn connecting these two Plantar arch 439 375 midpoints. The angle between this line and the edge of the table To assess whether the Dmanisi hominin foot possessed a longitu- 440 376 was used to determine the Proximal Articular Angle. The difference dinal plantar arch, we examined metatarsal torsion. In modern 441 377 between the Proximal and Distal Articular Angles was then calcu- humans, the plantar arch produces a transverse arch at the midfoot, 442 378 lated, giving the Tibial Torsion Angle. Lateral torsion (i.e., toeing with the base of the first metatarsal held above the ground plane and 443 379 “out”) was defined as positive and medial torsion (i.e., toeing “in”) the base of the fifth metatarsal resting on the ground plane. The major 444 380 was defined as negative, following previous research (Martin, 1957; axes of the proximal articular surfaces are thus radially arrayed in the 445 381 Hicks et al., 2007). This method is shown for the Dmanisi tibia coronal plane; metatarsal torsion changes this arrangement so that 446 382 (D3901) in Fig. 1A and B. the main axes of the distal articular surfaces are parallel to one 447 383 another and oriented in the sagittal plane, with the axis of rotation for 448 384 Analyses the metatarsal-phalangeal joints oriented horizontally (Fig. 2A). As 449 385 noted nearly a century ago by Morton (1922), the pattern of torsion 450 386 Proportions and relative hind limb length differs in apes, reflecting the lack of a transverse arch and the func- 451 387 We compared linear dimensions among species to examine the tional requirement of placing the first metatarsal in opposition to the 452 388 size and proportion of the Dmanisi hind limb elements. Addition- other rays (Fig. 2B) (see also Lewis,1980). We examined the pattern of 453 389 ally, summed lengths of the femur and tibia were used to provide metatarsal torsion in the Dmanisi hominins and compared it with the 454 390 a measure of total hind limb length for all specimens. This approach torsion patterns seen in apes and humans, as well as in the OH-8 foot. 455 391 ignores the additional hind limb length provided by the tarsals, but Note that other means of assessing the presence of a longitudinal 456 392 has the advantage of being applicable for specimens without plantar arch, such as cuboid or navicular morphology, could not be 457 393 a complete foot. We calculated a body size corrected Relative Hind employed in the Dmanisi sample. 458 394 Limb (RHL) length, using the formula RHL ¼ (Femur þ Tibia)/Body 459 395 Mass0.33. Calculating RHL this way assumes that limb length scales MetatarsalPROOF robusticity 460 396 isometrically with body mass. This assumption is supported in our First metatarsals in modern humans are substantially more 461 397 human sample [(Femur þ Tibia) ¼ 209.7(Estimated Mass)0.331, robust than those of the other rays, which may reflect the 462 398 r2 ¼ 0.40, n ¼ 86], although we note that limb length scales with mechanical stress experienced by the MTI during the second half of 463 399 negative allometry in our gorilla sample [(Femur þ Tibia) ¼ 200.7 the stance phase and toe-off (Griffin and Richmond, 2005). To 464 400 (Estimated Mass)0.250, r2 ¼ 0.83, n ¼ 22] and chimpanzee sample determine whether metatarsal robusticity is similar to that of 465 401 [(Femur þ Tibia) ¼ 303.3(Estimated Mass)0.157, r2 ¼ 0.30, n ¼ 60]. modern humans, we compared metatarsal robusticity in the 466 402 Body mass estimates for fossils were taken from the literature Dmanisi hominins with living humans and apes, and to available 467 403 (Table 1). Body mass estimates for modern humans and apes were hominin fossils. Metatarsal robusticity was calculated as (Dorso- 468 404 calculated using the intra Homo and Hominoid LSR regressions, plantar Midshaft Diameter2)/(Maximum Length Â Body Mass). This 469 405 respectively, for femoral head diameter, given in McHenry (1992). estimate of robusticity was chosen because, following standard 470 406 While this introduces some circularity since femoral dimensions are beam theory, the bending stress on the metatarsal shaft should 471 407 used for both hind limb length and body mass, given the importance increase linearly with metatarsal length and load (i.e., body mass), 472 408 of hind limb length in determining locomotor cost (Pontzer, 2005, while the resistance to bending should increase with the square of 473 409 2007a,b), RHL was nonetheless viewed as useful for comparing shaft diameter. Body masses were estimated from femoral head 474 410 hind limb length among species. It should be noted that other diameter (see above) or, for fossil specimens, taken from published 475 411 proxies of body mass generally give similar estimates of size, both in estimates of body size. For the Dmanisi sample, metatarsals 476 412 the Dmanisi sample (Lordkipanidze et al., 2007) and in extant robusticity was calculated using the body mass of the individual 477 413 478 414 Table 1 479 415 Long bone lengths and relative hind limb length (RHL) for fossil hominins, modern humans, chimpanzees, and gorillas. Q5 480

416 Taxon N Mass (kg) Humerus (mm) Femur (mm) Tibia (mm) RHL 481 417 482 A.L. 288a 27.9 237 281 241 174 418 KNM-WT 15,000b 51.0 319 429 380 221 483 419 KNM-ER 1472c 49.6 e 401 340 204 484 420 KNM-ER 1481c 57.0 e 396 333 215 485 c e 421 OH-34 51.0 432 367 218 486 OH-35d ee259 e 422 Dmanisi 48.8 295 382 306 191 487 423 Neanderthals 9 72.8 (9.2) e 433 (30) 342 (29) 189 (12) 488 424 Early modern humans 12 68.0 (7.9) e 471 (40) 401 (30) 217 (12) 489 425 Human F: 33UNCORRECTED 53.6 (5.2) 317 303 (19) 445 428 (27) 372 356 (28) 211 211 (13) 490 426 M: 53 67.9 (6.2) 331 (19) 463 (28) 387 (29) 211 (12) 491 Chimpanzee F: 40 39.4 (6.1) 301 299 (13) 295 292 (14) 251 247 (13) 159 161 (8) 427 M: 20 46.1 (7.5) 303 (14) 299 (13) 254 (11) 157 (7) 492 428 Gorilla F: 13 72.9 (12.3) 407 375 (19) 348 316 (14) 287 265 (11) 140 142 (5) 493 429 M: 9 134.5 (22.3) 439 (15) 380 (12) 310 (18) 137 (7) 494 430 Lengths are in millimeters with measurement code from Martin (1957) indicated; estimated masses are in kilograms. RHL is calculated as (femur þ tibia)/(estimated mass0.33); 495 431 see text. Dmanisi values are for the large adult individual (Lordkipanidze et al., 2007). Lengths in italics are estimates. Means (standard deviations) are shown for fossil and 496 432 extant groups. 497 a 433 Length estimates from Geissmann (1986), mass estimate from McHenry (1992). 498 b Length estimates from Ruff and Walker (1993); mass estimate from Ruff (2007). 434 c Length and mass estimates from Steudel-Numbers and Tilkens (2004). 499 435 d Length estimate from Susman and Stern (1982). 500

H. Pontzer et al. / Journal of Human Evolution xxx (2010) 1e13 5

501 Dmanisi hominins. We predicted a positive relationship between 566 502 tibia torsion and relative robusticity of metatarsal I, since greater 567 503 lateral torsion of the foot is expected to lead to greater loading of 568 504 the medial rays during walking and running. 569 505 570 506 Results 571 507 572 508 Linear dimensions and morphology 573 509 574 510 Femur and patella 575 511 The Dmanisi femur (D4167) appears to be functionally similar to 576 512 other Pleistocene Homo. The greater trochanter is less elevated than 577 513 the head but is laterally prominent. There is no groove for the 578 514 obturator externus tendon crossing the surface of the neck, which is 579 515 compressed anteroposteriorly (Lordkipanidze et al., 2007). Ante- 580 516 version (femoral torsion) is 8, slightly below the mean for most 581 517 human samples (e.g., Reikeras et al., 1983, mean ¼ 13, standard 582 518 deviation 7, n ¼ 47), but well within the range for modern humans 583 519 (À5 to þ30 , see Yushiok et al., 1987; Hermann and Egund, 1998). Q3 584 520 The shaft is straight in anterior view and displays the valgus 585 521 orientation (associated with a high bicondylar angle) typical of 586 522 hominins. The linea aspera is situated atop a well-developed 587 523 pilaster. The distal end is relatively large, with a maximum width of 588 524 the condyles of 75 mm. The patellar groove is deeply concave 589 525 transversely,PROOF but is vertically convex. Toward its lateral margin, the 590 526 patellar surface displays an area of smoothing, and tiny perforations 591 527 suggest loss of articular cartilage followed by eburnation of the 592 528 bone. This pathology is reflected also by evidence from the patella 593 529 (D3418), which is eburnated on the inferior portion of its lateral 594 Figure 2. A. Schematic diagram of the metatarsals in the average human foot in 530 595 anterior view (left foot shown). Torsion of the metatarsals (mean values shown) results articular surface. This osteoarthritis does not appear to have limited 531 from the radial arrangement of the proximal ends in the transverse arch and the knee function. 596 532 parallel arrangement of the distal ends at contact with the ground plane. B. A similar 597 533 diagram for the average chimpanzee foot. The proximal end of the metatarsal row Tibia 598 fi 534 contacts the substrate on the medial and lateral sides, and the distal rst ray is in Like the femur, the Dmanisi tibia (D3901) is robust, with large 599 opposition to the lateral rays. 535 proximal and distal articular ends relative to its length 600 536 (Lordkipanidze et al., 2007). The shaft is straight in the sagittal 601 537 with which they are associated (Table 3; see Lordkipanidze et al., plane, with very slight bowing in the coronal plane and an oval 602 538 2007). We used anterioreposterior (i.e., dorsal-plantar) midshaft cross-section at midshaft. The distal articulation is concave ante- 603 539 width in order to estimate bending strength in the sagittal plane, roposteriorly but flattened mediolaterally, and wider anteriorly 604 540 since bending stress in the metatarsal during walking and running (Fig. 1B). Anteriorly, the talar articulation exhibits squatting facets, 605 541 is expected to be greatest in the sagittal plane. One of the Dmanisi with both a crescent-shaped lateral facet and a smaller medial facet 606 542 third metatarsals, D2021, is nearly complete, but is broken at the present. These notches suggest contact with the talar neck during 607 543 base of the metatarsal head. To provide an estimate of robusticity extreme dorsiflexion of the foot at the ankle, as seen in populations 608 544 for this specimen, we estimated its length using the length of that regularly adopt a squatting posture (Singh, 1959). Posteriorly, 609 545 metatarsal IV, D2669, and the LSR equation relating metatarsal III the distal end exhibits a broad, channel-like groove for the tibialis 610 546 and IV lengths in our pooled sample of humans and apes posterior. Tibial torsion is very low (1, see below). 611 547 (MTIII ¼ 0.8835 MTIV þ 9.13; r2 ¼ 0.91, n ¼ 168, p < 0.001); the 612 548 estimated length (61 mm) is consistent with the morphology and Hind limb length and proportion 613 549 length of the specimen. Another specimen, D4058, a fifth meta- As noted in our initial description (Lordkipanidze et al., 2007), 614 550 tarsal, is also broken at the base of the head. The total length for this the Dmanisi hominins are of smaller stature than modern humans. 615 551 specimen was estimated at 62 mm, based on the preserved This is evident in the long bone dimensions. Comparing maximum 616 552 morphology of the head base. lengths of the femur and tibia, the Dmanisi hominins are absolutely 617 553 In our initial description, we suggested that the Dmanisi meta- larger than the A.L. 288 specimen of Australopithecus afarensis, the 618 554 tarsal I was less robust, relative to the other metatarsals, than is OH-35 specimen assigned to H. habilis, and living chimpanzees and 619 555 seen in humans, and that this mayUNCORRECTED be related to the lack of tibial gorillas, but substantially smaller than specimens assigned to H. 620 556 torsion in the Dmanisi population. Greater torsion of the tibia is erectus, as well as Neanderthals and modern humans (Table 1). RHL 621 557 expected to rotate the forefoot laterally, resulting in greater stress calculated from the Dmanisi femur and tibia is similarly interme- 622 558 on the medial margin of the foot during walking. In fact, plantar diate. Body mass for this individual is estimated at 48.8 kg with 623 559 pressure under the first ray (metatarsal I and hallux) exceeds that of a range of 46.9e50.8 kg (Lordkipanidze et al., 2007), giving an 624 560 any of the other metatarsals during normal human walking and estimated RHL of 191 with a range of 188e193. These RHL values 625 561 running (Hayafune et al., 1999; Nagel et al., 2008). To test the are greater than seen in living apes (gorillas: mean 140, standard 626 562 hypothesis that the increased tibial torsion seen in modern humans deviation Æ6.7; chimpanzees: 159 Æ 8.0) and the A.L. 288 A. afar- 627 563 relative to living apes is related to differences in relative metatarsal ensis specimen (174), but less than the KNM-ER 1481 and KNM-ER 628 564 robusticity, we plotted the degree of tibial torsion against the ratio 1472 specimens assigned to H. habilis (RHL of 215 and 204, 629 565 of robusticity in metatarsals I/III or I/IV for apes, humans, and the respectively) or the KNM-WT 15,000 and OH-35 African H. erectus 630

6 H. Pontzer et al. / Journal of Human Evolution xxx (2010) 1e13

631 Compared with more recent Homo, Dmanisi RHL is most similar to 696 632 our European Neanderthal sample (189 Æ 12.3) and below the 697 633 mean for fossil early modern humans (217 Æ 12.5) and modern 698 634 humans (211 Æ 12.6) (Table 1; Fig. 3A). The high RHL value for the 699 635 KNM-WT 15,000 specimen does not appear to be an artifact of its 700 636 juvenile status and estimates of adult hind limb length and body 701 637 mass for this specimen (Ruff and Walker, 1993) produce RHL values 702 638 in excess of 230. As noted in our initial report, the Dmanisi homi- 703 639 nins are like modern humans in their humero-femoral proportions. 704 640 When humerus length is plotted against femur length, Dmanisi 705 641 groups clearly with other members of the genus Homo (Fig. 3Bin 706 642 Lordkipanidze et al., 2007). 707 643 Crural index (100Â Tibia/Femur) for the Dmanisi specimen is 708 644 80.3, which is intermediate between European Neanderthals 709 645 (78.9 Æ 1.7) and the means for early modern humans (85.1 Æ 3.1) 710 646 and modern humans (83.5 Æ 3.1), and substantially below that of 711 647 the KNM-WT 15,000 H. erectus specimen (88.6). Together, these 712 648 measures suggest that the Dmanisi hominins exhibited the longer 713 649 hind limbs typical of Homo, albeit with RHL and crural index values 714 650 in the lower range of values typically observed in modern humans. 715 651 716 652 Talus 717 653 The Dmanisi talus is larger than those of living chimpanzees and 718 654 fossil specimens assigned to Australopithecus,aswellastheOH-8 719 655 H. habilisPROOFfoot (Table 2). Instead, in terms of size and morphology, the 720 656 Dmanisi talus most closely resembles that of later members of the 721 657 genus Homo, including living humans (Fig. 4). Like modern humans, 722 658 the trochlea of D4110 is strongly convex longitudinally, sellar in contour 723 659 and wider anteriorly than posteriorly. It lacks the relatively deep groove 724 660 evident in most chimpanzees and to a lesser extent in OH-8 (Fig. 4;see 725 661 Gebo and Schwartz, 2006). Its lateral and medial borders are about 726 662 equally elevated, and the articular surface does not slope toward the 727 663 inside of the foot. Medially, the facet for the malleolus extends forward 728 664 onto the neck but is relatively flat. There is no development of a cup- 729 665 shaped depression that would receive the malleolus during dorsi- 730 666 flexion, as in the footof apes (Aiello and Dean, 1990). The neck is stout 731 667 and expanded transversely. It appears slightly elongated relative to that 732 668 of recent Homo, but this elongation is not so pronounced as would be 733 669 usual for an ape. The (horizontal) angle subtended by the long axis of 734 670 the neck and the midline of the trochlea is similar to that in humans. 735 671 The inclination angle, measuring plantar inclination of the head and 736 672 neck relative to the plane of the lateral trochlea, is high and hence also 737 673 human-like. Although the head itself is incomplete, its morphology 738 674 suggests a symmetrical placement on the neck, and there is no indi- 739 675 cation of lateral rotation. On the superior aspect of the neck, there is 740 676 a small, flat surface situated laterally, just behind the head. Although 741 677 not clearly defined, this feature may be a squatting facet, comple- 742 678 mentary to depressions present on the distal tibia. 743 679 Posteriorly, the D4110 body presents two tubercles. The medial 744 680 tubercle is strong and projecting, so that the passage for the tendon 745 681 of flexor hallucis longus is channel-like. This channel has a slightly 746 682 747 683 748 Table 2 684 749 Talus dimensions, in millimeters. 685 Figure 3. A. Hind limb length (femur þ tibia) plotted against (estimated body 750 0.33 UNCORRECTED mass) . Gray diamonds: modern humans; gray circles: chimpanzees; open circles: 686 Specimen Species Talus 751 gorillas. Dashed lines are LSR equations for humans and apes (chimpanzees and 687 gorillas combined). Black square with white Â: Dmanisi; open triangles: African H. Length Head length 752 688 erectus (KNM-WT 15,000 and OH-34); black triangles: H. habilis (KNM-ER 1481 and A.L. 333-75 A. afarensis e 23.8 753 689 KNM-ER 1472); filled black square: A.L. 288. B. Metatarsal I length and C. metatarsal IV A.L. 288 A. afarensis 33.8 19.0 754 690 length versus femur length; symbols for extant groups as in A. Lengths for three KNM-ER 1464 H. erectus? 45.8 26.9 755 metatarsal I specimens are plotted for A. africanus (black squares; see Table 3) against KNM-ER 813 H. erectus? 47.3 e 691 estimate femur length for this species (333 mm) from Webb (1996). KNM-ER 1476 H. erectus? 41.3 25.3 756 692 OH-8 H. habilis 36.9 23.3 757 693 specimens (RHL of 221 and 218, respectively; Table 1). This result is Dmanisi 49.6 27.0 758 694 consistent with previous analyses (e.g., Jungers, 1982) indicating Human (n ¼ 14) 55.4 (3.7) 32.6 (2.6) 759 Chimpanzee (n ¼ 13) 38.3 (5.2) 21.4 (2.2) 695 short hind limbs in A. afarensis relative to modern humans. 760

H. Pontzer et al. / Journal of Human Evolution xxx (2010) 1e13 7

761 826 762 827 763 828 764 829 765 830 766 831 767 832 768 833 769 834 770 835 771 836 772 837 773 838 774 839 775 840 776 841 777 842 778 843 779 844 780 845 781 846

782 Figure 4. Trochlear profiles (white lines), and superior and inferior views of the Dmanisi talus with chimpanzee (chimp.), modern human and casts of other fossil tali. Trochlear 847 783 profiles are from Gebo and Schwartz (2006), except for Dmanisi and chimpanzee. A.L. 288 and KNM-ER 1464 have been mirror-imaged. 848 784 849 785 oblique (ape-like) rather than vertical (human-like) orientation, specimensPROOF is expanded, and the metatarsophalangeal articulation 850 786 but it is doubtful that this feature can be used to distinguish the extends upward and curves back onto the dorsal aspect of the shaft, 851 787 Dmanisi talus from modern homologues. The proximal articulation two features associated with human-like bipedal gait and reported 852 788 for the calcaneus, while less oval than seen in most modern previously for A. africanus (Susman and de Ruiter, 2004). The 853 789 humans, lacks the indentation seen in chimpanzees and to a lesser proximal articular surface in both D3442 and D2671 is divided into 854 790 extent in A.L. 288 (Fig. 4). D4110 does show some lateral projection two subequal components, a feature possibly related to the bipar- 855 fi 791 of the talo bular articulation, a trait associated with chimpanzees tite medial cuneiform associated with this population 856 792 rather than humans (Gebo and Schwartz, 2006), but the extent is (Lordkipanidze et al., 2007). Neither of these distinct facets is 857 793 similar to that of ER 1476, and not as extreme as ER 1464 (Fig. 4). deeply concave, but the lower presents a raised lateral border. 858 794 Notably, a similarly divided proximal articular surface is evident in 859 fi 795 Metatarsals the A.L. 333-54 A. afarensis rst metatarsal. As in australopithecines 860 796 In contrast to the talus, which is rather human-like, the Dmanisi and OH-8, the Dmanisi metatarsal I specimens are smaller than 861 fi 797 rst metatarsals are similar in size and morphology to earlier those of Neanderthals and modern humans (Table 2). Further, in the 862 798 hominins, including OH-8 and specimens assigned to Austral- Dmanisi specimens, the metatarsal I heads are relatively narrow, 863 799 opithecus. The proximal shaft in both Dmanisi metatarsal I not expanded mediolaterally as in modern humans (Fig. 5B). 864 800 865 801 866 802 867 803 868 804 869 805 870 806 871 807 872 808 873 809 874 810 875 811 876 812 877 813 878 814 879 815 UNCORRECTED 880 816 881 817 882 818 883 819 884 820 885 821 886 822 887 fi 823 Figure 5. Comparison of metatarsal morphology. A. Pro le view, Dmanisi metatarsals I, III, IV and V (middle column) compared with fossil hominins, humans, and chimpanzees. 888 Top two rows: metatarsal I; third row, metatarsal III; fourth row, metatarsal IV; fifth row, metatarsal V. D4058 image is generated from a CT scan. Metatarsal V specimens have been 824 mirrored to aid visual comparison with other metatarsals. Hatched area on human MTV is clay used to stabilize specimen during scanning. B. Metatarsal I heads. Scale bar: 1 cm. 889 825 Adapted from Susman and de Ruiter (2004). 890

8 H. Pontzer et al. / Journal of Human Evolution xxx (2010) 1e13

891 The Dmanisi central and lateral metatarsals, like the metatarsal I 956 892 specimens, have straight shafts in mediolateral view, and appear 957 893 functionally similar to those of modern humans (Fig. 5A). However, 958 894 the central and lateral metatarsals appear to be relatively longer, 959 895 compared with the Dmanisi metatarsal I specimens, than is typical 960 896 of modern humans. While caution must be exercised given the 961 897 small sample size and estimation of lengths for some elements, the 962 898 Dmanisi metatarsals IIIeVare25e31% longer than the metatarsal I 963 899 specimens (Table 3). This difference is similar to that seen in 964 900 chimpanzees and gorillas, in which metatarsals IIIeV are an 965 901 average of 24e28% (chimpanzees) and 31e36% (gorillas) longer 966 902 than metatarsal I (Table 3). By contrast, human metatarsals III and 967 903 IV average 14e15% longer than metatarsal I, and the human 968 904 metatarsal V is only 4% longer, on average, than metatarsal I (Table 969 905 3). The length of the Dmanisi foot relative to that of the hind limb 970 906 appears essentially modern, with ratios of metatarsal I and IV 971 Figure 6. Boxplot showing metatarsal robusticity, calculated as (dorsoplantar midshaft 907 length to femur length similar to those of modern humans (Fig. 3B 972 diameter)2/(length Â estimated mass). Gray boxes: gorillas (n ¼ 20); white boxes: 908 and C). Among hominoids, species differences in metatarsal/femur chimpanzees (n ¼ 60); black boxes: humans (n ¼ 86); black squares with white Â: 973 909 proportion derive primarily from increased femur length in homi- Dmanisi. Boxes indicate 25th, 50th, and 75th percentiles. Whiskers indicate sample 974 910 nins; the range of metatarsal lengths is similar across chimpanzees, range, excluding outliers. 975 911 gorillas, and humans (Fig. 3B and C). 976 912 977 body mass for this species (40.8 kg, using the intra-human 913 978 formulae in McHenry, 1992) all fall above the mean for modern 914 Metatarsal robusticity 979 humans (Table 3), with the highest value exceeding the maximum 915 980 robusticityPROOF value in our human sample (6.9). These robusticity 916 Robusticity in the first metatarsals from Dmanisi (D3442: 4.9, 981 values remain high even when the intra-hominoid equation is used 917 D2671: 5.8) fell in the upper range of values for our modern human 982 to estimate body mass (52.8 kg), and are of course much higher if 918 sample (4.52 Æ 0.72 n ¼ 86), and well above the means for chim- 983 the female estimates for body mass are used. 919 panzees (3.81 Æ 0.67 n ¼ 60) and gorillas (2.10 Æ 0.68 n ¼ 20) 984 Robusticity was greater for the Dmanisi metatarsal III (D2021: 920 (Fig. 6). Robust first rays appear to be common among all hominins. 985 2.7) and metatarsal IV (D2669: 3.0) specimens when compared 921 The robusticity values for three metatarsal I specimens assigned to 986 with living humans. Metatarsal III robusticity in the Dmanisi 922 A. africanus (4.8, 6.7, and 7.6), calculated using the estimated male 987 sample was greater than 99% of the human specimens (1.8 Æ 0.31 923 988 n ¼ 86), near the mean for chimpanzees (2.8 Æ 0.56 n ¼ 60; Fig. 6). 924 989 Table 3 Metatarsal IV robusticity in Dmanisi was greater than 90% of the 925 990 Metatarsal dimensions. Means (standard deviations) shown for extant groups. human specimens (2.0 Æ 0.51 n ¼ 86) and also exceeded the 926 991 Q6 chimpanzee mean (2.1 Æ 0.43 n ¼ 60). In contrast, the Dmanisi 927 Species Specimen Length Shaft AP Dia. Robusticity 992 metatarsal V robusticity (D4058: 1.5) fell well below the mean for 928 Metatarsal I 993 A. africanusb SK 1813 41.4 10.6 6.7 modern humans (2.2 Æ 0.56 n ¼ 86), and closer to the mean for 929 994 A. africanusb SKX 5017 43.5 11.6 7.6 chimpanzees (1.5 Æ 0.35 n ¼ 60). The pattern of robusticity evident 930 b 995 A. africanus Stw 562 50.7 10.0 4.8 in the Dmanisi metatarsals, with the fifth metatarsal having the 931 Neanderthala Shanidar 4 60.6 12.9 3.9 996 a lowest robusticity, is very unusual in humans and is more common 932 Neanderthal La Ferrassie 1 60.5 11.7 2.7 997 c in apes (Table 3; see also Archibald et al., 1972). Further, while 933 Dmanisi D2671 47.2 10.6 5.8 998 D3442 47.0 9.6 4.9d caution must be exercised in interpreting robusticity in the Dmanisi 934 999 Human (n ¼ 86) 62.3 (4.5) 13.2 (1.3) 4.5 (0.7) metatarsals given the estimation of lengths and body masses, it 935 Chimpanzee (n ¼ 60) 53.4 (2.8) 9.1 (0.9) 3.8 (0.7) 1000 should be noted that the pattern of robusticity does not change 936 Gorilla (n ¼ 22) 56.6 (6.4) 10.3 (1.2) 2.1 (0.7) 1001 when mass and length estimates are varied Æ10%. 937 Metatarsal III 1002 938 Dmanisi D3479 e 6.7 e 1003 939 D2021 61 9.0 2.7e Metatarsal robusticity and tibial torsion 1004 940 Human (n ¼ 86) 72.0 (5.3) 8.9 (0.9) 1.8 (0.3) 1005 Chimpanzee (n ¼ 60) 68.2 (4.1) 8.8 (0.6) 2.8 (0.6) 941 þ 1006 Gorilla (n ¼ 22) 74.1 (7.3) 10.3 (1.3) 1.6 (0.4) Torsion in the Dmanisi tibia is very low ( 1 ; see Fig. 1) 942 compared with modern humans (15.3 Æ 8.9, n ¼ 86), and high 1007 943 Metatarsal IV compared with chimpanzees (À8.4 Æ 7.9, n ¼ 60) and gorillas 1008 Dmanisi D2669 59.1 8.6 3.0c À Æ ¼ 944 Human (n ¼ 86) 71.1 (5.4) 9.3 (1.4) 2.0 (0.5) ( 18.9 6.2 n 22) (Table 1). Note that this value of tibial torsion 1009 945 Chimpanzee (n ¼ 60) 66.8UNCORRECTED (4.2) 7.5(0.6) 2.1(0.4) is different than the incorrect value reported initially 1010 946 Gorilla (n ¼ 22) 74.8 (7.2) 9.6(1.3) 1.4(0.4) (Lordkipanidze et al., 2007). The degree of torsion in the Dmanisi 1011 947 Metatarsal V tibia is lower than all but one specimen from our modern human 1012 948 Dmanisi D4058 62 6.8 1.5e sample (Fig. 7). In contrast, tibial torsion in the Nariokotome 1013 949 Human (n ¼ 86) 64.8 (5.0) 9.3 (1.2) 2.2 (0.6) specimen KNM-WT 15,000 (34) and other Pleistocene hominins is 1014 ¼ 950 Chimpanzee (n 60) 66.4 (4.4) 6.3 (0.6) 1.5 (0.4) at or above the mean for modern humans. While caution must be 1015 Gorilla (n ¼ 22) 77.2 (9.4) 8.2 (1.4) 1.0 (0.3) 951 used in interpreting tibial torsion from reconstructed specimens, 1016 a 952 Dimensions taken from casts. such as KNM-WT 15,000 with its hafted distal epiphysis, torsion in 1017 b Dimensions taken from Susman and de Ruiter (2004). 953 the Dmanisi tibia clearly falls well below that of other Pleistocene 1018 c Body mass: 41.2 kg (Lordkipanidze et al., 2007). 954 d Body mass: 40.2 kg (Lordkipanidze et al., 2007). specimens. Further, it should be noted that femoral torsion in the 1019 955 e Body mass: 48.8 kg (Lordkipanidze et al., 2007). Dmanisi hind limb does not compensate for the lack of tibial 1020

H. Pontzer et al. / Journal of Human Evolution xxx (2010) 1e13 9

1021 1086 1022 1087 1023 1088 1024 1089 1025 1090 1026 1091 1027 1092 1028 1093 1029 1094 1030 1095 1031 1096 1032 1097 1033 1098 1034 1099 1035 1100 1036 1101 1037 1102 1038 1103 1039 1104 1040 1105 1041 1106 1042 1107 1043 Figure 7. Tibial torsion. Lateral torsion is positive; medial is negative. Boxes indicate 1108 25th, 50th, and 75th percentiles. Whiskers indicate sample range, excluding outliers. 1044 1109 Data for middle Pleistocene Homo (Broken Hill) and Neanderthals (Kiik-Koba and 1045 Shanidar) from Wallace et al. (2008). PROOF 1110 1046 1111 1047 1112 1048 torsion. The combined femoral þ tibial torsion in the Dmanisi hind 1113 1049 limb results in a net À7 rotation (intoeing), well below typical net 1114 1050 rotation in modern humans (þ20 , Rittmeister et al., 2006). 1115 1051 Plotting tibial torsion against the relative robusticity of the first 1116 1052 and lateral rays, it is apparent that humans exceed chimpanzees 1117 1053 and gorillas in terms of both torsion and relative robusticity of the 1118 1054 first metatarsal (Fig. 8). Here again, the Dmanisi hominins are 1119 1055 intermediate between chimpanzees and humans in both tibial 1120 1056 torsion and metatarsal robusticity. However, while there is 1121 a correlation among species between tibia torsion and relative 1057 Figure 8. A. The ratio of metatarsal I robusticity to metatarsal III robusticity plotted 1122 2 < 2 1058 metatarsal robusticity (MTI/III: r ¼ 0.35, p 0.01; MTI/IV: r ¼ 0.57, against tibia torsion. B. The ratio of metatarsal I robusticity to metatarsal IV robusticity 1123 1059 p < 0.01; n ¼ 169 with species pooled), there is no significant plotted against tibia torsion. Open circles: gorillas; gray circles: chimpanzees, black 1124 1060 correlation within species (p > 0.05 all comparisons). Thus, while circles: humans; black square with white Â, Dmanisi. Dmanisi values are calculated 1125 using both D2671 and D3442 first metatarsals. 1061 metatarsal robusticity does appear to correspond with tibia torsion 1126 1062 among species, these variables do not appear to be linked within 1127 1063 species. Discussion 1128 1064 1129 1065 Plantar arch Dmanisi biomechanics and the origin of Homo 1130 1066 1131 1067 Metatarsal torsion in the Dmanisi hominins is similar to that Hypotheses for the emergence of the genus Homo often propose 1132 1068 seen in modern humans (Fig. 9A; Table 4). The first metatarsals that the derived locomotor anatomy seen in early members of the 1133 1069 of humans and chimpanzees are significantly different in terms of genus reflects increased ranging due to increased meat consump- 1134 1070 torsion (p ¼ 0.006 Student’s two-tailed t-test), but the range tion and selection for improved economy and endurance (Shipman 1135 1071 of variation in both species is substantial. Similarly, mean torsion in and Walker, 1989; Bramble and Lieberman, 2004; Pontzer, 2006). 1136 1072 metatarsal V is statistically different between humans and chim- The Dmanisi hominins provide an opportunity to examine the 1137 1073 panzees (p ¼ 0.04), but the ranges overlap considerably. However, possible effects of carnivory on post-cranial anatomy without the 1138 1074 torsion in the second, third, and fourth metatarsals are distinctly confounding effects of heat stress and increased body and brain size 1139 1075 different between species (p < UNCORRECTED0.001 all comparisons). While present in East African populations of Pleistocene H. erectus. Results 1140 1076 torsion of the Dmanisi first and fifth metatarsals is within the range of this study suggest that, despite a number of primitive retentions 1141 1077 of values seen in both chimpanzees and humans, torsion in the in foot morphology, the Dmanisi hominins were more cursorially 1142 1078 Dmanisi metatarsal III and IV falls within the human range, well adapted than earlier hominins. 1143 1079 outside of the chimpanzee range. A similar pattern of torsion is Among terrestrial species, the greatest single anatomical 1144 1080 evident in the OH-8 foot (Fig. 9A). For both the Dmanisi and Olduvai predictor of locomotor economy is effective limb length, the length 1145 1081 specimens, a human-like pattern of metatarsal torsion is likely and of the hind limb as a strut (Kram and Taylor, 1990; Pontzer, 2005, 1146 1082 this indicates the presence of a human-like transverse arch 2007a,b). In fact, limb length drives the scaling of mass-specific 1147 1083 (Fig. 9B), because the absence of a transverse arch would bring the locomotor cost (i.e., metabolic energy per kilogram body mass per 1148 1084 functional axes of the metatarsal-phalangeal joints out of align- distance traveled) from ants to elephants (Pontzer, 2007a), and is 1149 1085 ment (Fig. 9C). a better predictor of mass-specific locomotor cost than body mass. 1150

10 H. Pontzer et al. / Journal of Human Evolution xxx (2010) 1e13

1151 hominins were intermediate between the australopithecines and 1216 1152 later members of the genus Homo in terms of locomotor economy. 1217 1153 Relative to body mass, the Dmanisi hind limb is clearly longer than 1218 1154 that of African apes and the A.L. 288 A. afarensis specimen. In fact, 1219 1155 the Dmanisi specimen is within the lower range of values for 1220 1156 modern humans (Table 1, Fig. 3A). 1221 1157 While Dmanisi metatarsal morphology differs somewhat from 1222 1158 that of later Homo (Fig. 5; Table 3), the Dmanisi foot appears func- 1223 1159 tionally similar to that of modern humans. Among our comparative 1224 1160 sample, the size and morphology of the Dmanisi talus is most like 1225 1161 that of African H. erectus and modern humans (Table 2, Fig. 4), with 1226 1162 a trochlea that is broad and flat (unlike OH-8). This suggests 1227 1163 a human-like ankle joint with increased surface area for trans- 1228 1164 mitting joint reaction forces associated with walking and running 1229 1165 (DeSilva, 2009). Further, the pattern of metatarsal torsion indicates 1230 1166 the presence of a human-like midfoot transverse arch (Fig. 9B), since 1231 1167 the lack of a transverse arch would require that the metatarsal- 1232 1168 phalangeal joints of the lateral rays splay laterally, a condition that is 1233 1169 functionally implausible and unseen in humans or other apes 1234 1170 (Fig. 9C). The presence of a midfoot transverse arch in turn indicates 1235 1171 the presence of a longitudinal plantar arch and a concomitant 1236 1172 improvement in locomotor efficiency (Ker et al., 1987; Alexander, 1237 1173 1991; Bramble and Lieberman, 2004). Without a calcaneus, cuboid, 1238 1174 and navicular, it is impossible to know whether the arch of the 1239 1175 DmanisiPROOF foot was similar in some critical aspects, such as an 1240 1176 immobile (close-packed) calcaneal-cuboid articulation, to that of 1241 1177 later hominins (Harcourt-Smith and Aiello, 2004). However, the 1242 1178 talar morphology, presence of an arch, and an adducted, robust first 1243 1179 metatarsal suggest the Dmanisi foot was fully committed to terres- 1244 1180 trial bipedalism and functionally equivalent, in terms of rigidity 1245 1181 during stance phase and toe-off, to that of modern humans. 1246 1182 With a relatively long hind limb, arched foot, fully adducted and 1247 1183 robust first ray, and human-like ankle joint, the Dmanisi hind limb 1248 1184 appears to have been similar in most functional aspects to modern 1249 1185 humans. Relative to the australopithecines, the Dmanisi hominins 1250 1186 evince improved economy and efficiency in both walking and 1251 1187 running. Since the Dmanisi hominins are associated with clear 1252 1188 evidence of stone tool use and butchery (Lordkipanidze et al., 1253 1189 2007), their cursorial adaptations support the hypothesis that the 1254 1190 adoption of meat eating in early Homo, either through hunting or 1255 1191 scavenging, resulted in selection for more economical walking and 1256 1192 running. Other proposed pressures, namely warmer temperatures 1257 1193 (Walker, 1993) and increased body and brain size (Lovejoy, 1999) 1258 Figure 9. A. Boxplots of metatarsal torsion in chimpanzees (gray) and humans (white), 1194 1259 compared with Dmanisi (black square with white Â) and OH-8 (black diamonds). were absent for these hominins. 1195 Boxes indicate 25th, 50th, and 75th percentiles and whiskers indicate sample ranges, 1260 1196 excluding outliers. Positive values indicate medial rotation of the distal end. B. and C. Locomotor evolution in the genus Homo 1261 1197 Schematic diagram of the Dmanisi foot. B. AP projection with a transverse arch. C. AP 1262 projection with no transverse arch. See also Fig. 2. 1198 While our analyses focus on locomotor economy in the Dmanisi 1263 1199 Species with particularly long limbs for their body mass have hominins, numerous and sometimes competing evolutionary 1264 1200 a relatively low cost of transport (i.e., energy spent per distance), pressures undoubtedly act in concert to shape locomotor anatomy. 1265 1201 while species with short limbs have high locomotor costs (Pontzer, Indeed, the low crural index of the Dmanisi hind limb may be 1266 1202 2007a). The effect of limb length on cost is also evident within indicative of competing selection pressures. While the hind limb 1267 1203 species (Minetti et al., 1994; Steudel-Numbers and Tilkens, 2004; overall is longer than in australopithecines, the tibia is relatively 1268 1204 Pontzer, 2007b). Limb length comparisons suggest the Dmanisi short, which may be a response to the cold winter temperatures 1269 1205 UNCORRECTED 1270 1206 1271 1207 Table 4 1272 1208 Metatarsal torsion. Estimates from incomplete specimens are in italics. Means (standard deviation) shown for extant groups. 1273 1209 Species Torsion (degrees) 1274 1210 1275 Specimen metatarsal I II III IV V 1211 1276 OH-8 10 À724 25 e 1212 Dmanisi D2671 3 e D3479 35 D2669 29 D4058 7 1277 1213 D3442 15 D2021 38 1278 1214 Human (n ¼ 10) 2.2 (11.5) 5.6 (8.2) 20.4 (9.6) 23.6 (7.1) 15.3 (4.6) 1279 1215 Chimpanzee (n ¼ 9) 19.1 (11.6) À36.1 (9.3) À7.6 (6.6) À0.1 (2.5) 6.9 (10.1) 1280

H. Pontzer et al. / Journal of Human Evolution xxx (2010) 1e13 11

1281 (Trinkaus, 1981) typical of the southern Caucasus (see bipedalism, in lateral view the Dmanisi metatarsal I specimens are 1346 1282 Supplementary Information). Conversely, the longer limbs and high more similar to those of OH-8, as well as specimens assigned to A. 1347 1283 crural index in KNM-WT 15,000 may reflect the aligned pressures africanus (Susman and de Ruiter, 2004), than to modern humans 1348 1284 of locomotor economy and thermoregulation in that population. In (Fig. 5A). Further, the phalangeal articulation of the Dmanisi first 1349 1285 addition, the small, broad pelvis from Gona, Ethiopia, dated to metatarsals is tall and narrow, like that of australopithecines, and 1350 1286 between 0.9 and 1.4 mya (Simpson et al., 2008), underscores the lacks the mediolateral expansion seen in modern humans (Fig. 5B). 1351 1287 importance of neonatal head size and mechanics of parturition in The degree of torsion in the Dmanisi tibia (1) also differs 1352 1288 shaping hominin locomotor anatomy, particularly as brain size substantially from the modern human mean (15.3). It is lower than 1353 1289 increased through the Pleistocene. Parsing the independent effects all but 1% of the humans in our sample and lower than that of other 1354 1290 of these and other selection pressures on the hominin locomotor Pleistocene hominins (Fig. 7). 1355 1291 skeleton, as well as identifying patterns of pleiotropy and other The high relative robusticity of the central metatarsals III and IV, 1356 1292 non-adaptive change, remains an important goal for those recon- as well as the low robusticity of the Dmanisi metatarsal V (Fig. 6), 1357 1e4 1293 Q4 structing hominin locomotor evolution. suggests a loading regime in the Dmanisi that is different than in 1358 1294 The results of this study support the hypothesis that the adop- modern humans. In our initial report (Lordkipanidze et al., 2007), 1359 1295 tion of carnivory led to selection for improved terrestrial biped- we suggested that the greater robusticity of the lateral metatarsals 1360 1296 alism and the post-cranial changes seen in early Pleistocene Homo, (IIIeV) in the Dmanisi hominins may be related to the lack of tibial 1361 1297 but determining the precise timing and extent of evolutionary torsion, since the absence of lateral tibial torsion will tend to rotate 1362 1298 change in the hominin hind limb through the late Pliocene and the foot medially relative to modern humans (Fig.10), which should 1363 1299 early Pleistocene remains difficult. Comparisons to the australo- result in increased plantar pressures under the lateral rays during 1364 1300 pithecines are limited to a small number of specimens of A. afar- walking and running. Our data provide only weak support for this 1365 1301 ensis and A. africanus that are both temporally and geographically hypothesis. Tibial torsion and the relative robusticity of the central 1366 1302 distant, while elements for early Pleistocene hominins are scarce rays (III and IV) are correlated across hominoids, but are not 1367 1303 and generally fragmentary. For example, the RHL estimates for correlated within humans, chimpanzees, or gorillas (Fig. 8). Further, 1368 1304 KNM-ER 1481 and KNM-ER 1472, typically assigned to H. habilis humans, which have the highest degree of tibial torsion, also have 1369 1305 and marginally older than the Dmanisi fossils (Klein, 1999), may the highestPROOF average metatarsal V robusticity, while the Dmanisi 1370 1306 suggest that increased hind limb length preceded the hominin metatarsal V robusticity is comparatively low (Fig. 6). 1371 1307 expansion into Eurasia. However, limb proportions for H. habilis are At least two issues complicate the relationship between tibial 1372 1308 uncertain (Haeusler and McHenry, 2004), making it difficult to torsion and metatarsal robusticity. First, as noted in a previous 1373 1309 assess whether the Dmanisi hominins are more or less derived in critique of this hypothesis (Wallace et al., 2008), other variables, 1374 1310 terms of hind limb length. Comparing the Dmanisi and OH-8 foot is such as femoral anteversion, affect the position of the foot, and it 1375 1311 useful but inconclusive. The OH-8 specimen is similar in metatarsal may be that tibial torsion by itself is a poor predictor of foot position 1376 1312 morphology and the presence of an arch, but seemingly more and metatarsal loading. Second, the relative robusticity of meta- 1377 1313 primitive in talar morphology and overall size. The combination of tarsals IIeV does not appear to correlate strongly with the relative 1378 1314 derived and primitive features in OH-8 and the Dmanisi foot magnitudes of strain experienced during walking and running in 1379 1315 highlights the complex nature of morphological evolution in the humans (Griffin and Richmond, 2005). For example, plantar pres- 1380 1316 hominin hind limb (Harcourt-Smith and Aiello, 2004) and under- sure readings during walking and running in humans (Hayafune 1381 1317 scores the need for more information before competing evolu- et al., 1999; Nagel et al., 2008), as well as in vitro strain measures 1382 1318 tionary scenarios, either the simple carnivory model discussed here during simulated walking in cadaveric feet (Donahue and Sharkey, 1383 1319 or others, can be assessed with greater confidence. 1999), indicate that stresses are greater in metatarsal II than 1384 1320 metatarsal V, but the robusticity of the fifth metatarsal significantly 1385 1321 exceeds that of the second (Griffin and Richmond, 2005). Further, 1386 Foot mechanics of early Homo 1322 soft tissues, including the plantar fascia and digital flexors, affect 1387 1323 the magnitude of stresses experienced by the metatarsals 1388 Dmanisi is the only early Pleistocene hominin population for 1324 (Donahue and Sharkey, 1999). Thus, while we find it unlikely that 1389 which a complete femur, tibia, and associated foot bones have been 1325 tibial torsion is unrelated to foot position or that foot position is 1390 found, and it is therefore useful in establishing the pattern of hind 1326 unrelated to metatarsal loading regime, a more sophisticated 1391 limb traits evident in early Homo. As discussed above, the hind limb 1327 model of mechanical loading in the forefoot and a better under- 1392 appears to be functionally similar to later members of the genus 1328 standing of non-mechanical influences on metatarsal morphology 1393 Homo, yet metatarsal morphology and tibial torsion are relatively 1329 are needed to understand how tibial rotation and metatarsal 1394 primitive. The metatarsals appear to be similar in size and 1330 robusticity reflect the locomotor mechanics and evolutionary 1395 morphology to OH-8 and earlier hominins, and less like those of 1331 history of the Dmanisi hominins. Future work might examine the 1396 modern humans. The lengths of metatarsals III, IV and V relative to 1332 effect of net long bone rotation (i.e., femur þ tibia) and tarsal 1397 metatarsal I appear to be more similar to the condition seen in apes 1333 morphology on plantar pressure distribution in living humans. The 1398 than in modern humans (Table 3). While the Dmanisi metatarsal I is 1334 effect of lateral foot rotation on locomotor performance also 1399 robust and morphologically commensurate with human-like 1335 UNCORRECTEDwarrants further study. The limited work on this topic has sug- 1400 1336 gested that improved sprint performance is correlated with a low 1401 1337 positive degree of lateral foot rotation (Fuchs and Staheli, 1996). 1402 1 When the rigidity of the arch is effectively compromised, as during walking 1338 1403 over loose sand (Lejeune et al., 1998), the effort to move the center of mass and the The similarities between the OH-8 and Dmanisi feet suggest that 1339 energetic cost of walking increases significantly. the primitive retentions evident in both may have been common 1404 1340 2 Here, we follow the International Commission on Stratigraphy in placing the among populations of Homo in the early Pleistocene. The more 1405 1341 base of the Pleistocene at 2.59 mya. derived foot anatomy indicated by the hominin footprints at Ileret, 1406 3 1342 Landmark-based estimates, following the Martin (1957) protocol, give a range dated to 1.5 mya (Bennett et al., 2009) suggests that these primitive 1407 of torsion values from À2 to þ2. 1343 retentions were lost later, as hominin locomotor evolution 1408 4 Regrettably, this critique used a torsion value of 21.9 for the Dmanisi tibia, 1344 reflecting an error in our initial report (Lordkipanidze et al., 2007). As noted above, continued through the Pleistocene. The primitive features of the 1409 1345 the correct value is 1 (see Table 1 and Fig. 1). Dmanisi and OH-8 feet might also help explain some of the features 1410

12 H. Pontzer et al. / Journal of Human Evolution xxx (2010) 1e13

1411 1476 1412 1477 1413 1478 1414 1479 1415 1480 1416 1481 1417 1482 1418 1483 1419 1484 1420 1485 1421 1486 1422 1487 1423 1488 1424 1489 1425 1490 1426 1491 1427 1492 1428 1493 1429 1494 1430 Figure 10. Superior views of the foot in A. Neanderthals (La Ferrassie 1), B. modern humans, and C. Dmanisi (composite from CT-scans), showing the effect of tibial torsion on foot 1495 position. The dashed line, indicating the lateral torsion of the tibia, is aligned here with the trochlea of the talus. Lateral rotation of the foot in Pleistocene hominins and modern Q7 1431 humans aligns the first ray with the direction of travel (solid line), and the greatest plantar pressures are experienced by the first metatarsal during the toe-off portion of stance 1496 1432 phase in walking and running. The absence of tibial torsion in the Dmanisi hominins is expected to result in relatively greater stresses for the lateral rays compared with humans 1497 1433 and other Pleistocene hominins. D. OH-8 (from CT-scans of casts), and E. STW 573 (from Clarke and Tobias, 1995) are also shown. Scale bar: 5 cm. 1498 1434 1499 seen in the H. floresiensis foot (Jungers et al., 2009). If the population Ocobock assisted with manuscript preparation. This work was 1435 1500 from which H. floresiensis diverged was relatively primitive in its supportedPROOF by the Georgian National Science Foundation, a Rolex 1436 1501 foot morphology, fewer evolutionary changes might be needed to Award for Enterprise, BP Georgia, the Fundación Duques de Soria, 1437 1502 produce the distinct set of traits seen in the Liang Bua foot. and the Swiss National Science Foundation. Support was also 1438 1503 provided by the Washington University Department of Anthro- 1439 1504 pology, the Harvard University Department of Anthropology, 1440 Conclusion 1505 a Harbison Faculty Fellowship to HP, a National Science Foundation 1441 1506 Doctoral Dissertation Improvement Grant (BCS 0647624) to CR, and 1442 Analyses of the Dmanisi skulls have demonstrated that these 1507 National Science Foundation, Leakey Foundation, and American 1443 hominins are primitive in many respects relative to other early 1508 Philosophical Society awards to GPR. 1444 Pleistocene Homo, and similar in some cranial dimensions, 1509 1445 including endocranial volume, to H. habilis (Vekua et al., 2002; 1510 Rightmire et al., 2006). We find this parallel echoed in the func- 1446 Appendix. Supplementary data 1511 1447 tional morphology of the Dmanisi hind limb with its mosaic of 1512 primitive and derived traits. The presence of an arch, human-like 1448 Supplementary data associated with this article can be found in 1513 talus, and increased relative hind limb length in this population are 1449 the online version, at doi:10.1016/j.jhevol.2010.03.006. 1514 1450 suggestive of selection for improved locomotor economy and effi- 1515 1451 ciency. These traits, along with the numerous stone artifacts and 1516 1452 taphonomic traces that provide evidence for butchery at the site, References 1517 1453 are consistent with the hypothesis that early Homo was adapted to 1518 1454 some degree of carnivory (hunting, scavenging, or both) and the Aiello, L., Dean, C., 1990. An Introduction to Human Evolutionary Anatomy. 1519 increased locomotor demands that this foraging strategy entails Academic Press, San Diego. 1455 Alemseged, Z., Spoor, F., Kimbel, W.H., Bobe, R., Geraads, D., Reed, D., Wynn, J.G., 1520 1456 (Shipman and Walker, 1989; Bramble and Lieberman, 2004; 2006. A juvenile early hominin skeleton from Dikika, Ethiopia. Nature 443, 1521 1457 Carbone et al., 2005; Pontzer, 2006). Further, the location of 296e301. 1522 Dmanisi, in an open, temperate habitat far from the African tropics, Alexander, R.M., 1991. Energy saving mechanisms in walking and running. J. Exp. 1458 Biol. 160, 55e69. 1523 1459 strengthens the hypothesis that this foraging strategy was critical Archibald, J.D., Lovejoy, C.O., Heiple, K.G., 1972. Implications of relative robusticity in 1524 1460 in the expansion of early Homo throughout Africa and into Asia the Olduvai Metatarsus. Am. J. Phys. Anthropol. 37, 93e95. 1525 (Shipman and Walker, 1989). Intriguingly, the Dmanisi hominins Bennett, M.R., John, W.K., Harris, J.W.K., Richmond, B.G., Braun, D.R., Mbua, E., 1461 Kiura, P., Olago, D., Kibunjia, M., Omuobo, C., Behrensmeyer, A.K., Huddart, D., 1526 1462 are less derived in terms of hind limb length, and possibly meta- Gonzalez, C., 2009. Early hominin foot morphology based on 1.5-million-year- 1527 1463 tarsal morphology, than African H. erectus specimens roughly old footprints from Ileret, Kenya. Science 323, 1197e1201. 1528 1464 200,000 years younger (KNM-WT 15,000). This may suggest that Bramble, D.M., Lieberman, D.E., 2004. Endurance running and the evolution of 1529 Homo. Nature 432, 345e352. selection pressure for improved walking and running performance 1465 UNCORRECTEDBrowning, R.C., Modica, J.R., Kram, R., Goswami, A., 2007. The effects of adding mass 1530 1466 continued through the early and middle Pleistocene. More fossils to the legs on the energetics and biomechanics of walking. Med. Sci. Sports 1531 e 1467 from this period, sampled from more localities, will help elucidate Exerc. 39, 515 525. 1532 the undoubtedly complicated origins of our genus, and provide Carbone, C., Cowlishaw, G., Isaac, N.J.B., Rowcliffe, J.M., 2005. How far do animals 1468 go? Determinants of day range in mammals. Am. Nat. 165, 290e297. 1533 1469 a more complete perspective on the early Pleistocene population at Clarke, R.J., Tobias, P.V., 1995. Sterkfontein Member 2 foot bones of the oldest South 1534 1470 Dmanisi. African hominid. Science 269, 521e524. 1535 Conroy, G.C., 2005. Reconstructing Human Origins: a Modern Synthesis, second ed. 1471 Norton, New York. 1536 1472 Acknowledgements DeSilva, J.M., 2009. Functional morphology of the ankle and the likelihood of 1537 1473 climbing in early hominins. Proc. Natl. Acad. Sci. U.S.A. 106, 6567e6572. 1538 Donahue, S.W., Sharkey, N.A., 1999. Strains in the metatarsals during the stance 1474 We thank David Raichlen, Daniel Lieberman, and three phase of gait: implications for stress fractures. J. Bone Joint Surg. 81, 1236e1243. 1539 1475 reviewers for comments that improved this manuscript. Cara Fuchs, R., Staheli, L.T., 1996. Sprinting and intoeing. J. Pediatr. Orthop. 4, 489e491. 1540

H. Pontzer et al. / Journal of Human Evolution xxx (2010) 1e13 13

1541 Garland Jr., T., 1983. Scaling the ecological cost of transport to body mass in Pontzer, H., 2005. A new model predicting locomotor cost from limb length via 1595 1542 terrestrial mammals. Am. Nat. 121, 571e587. force production. J. Exp. Biol. 208, 1513e1524. 1596 Gebo, D.L., Schwartz, G.T., 2006. Foot bones from Omo: implications for hominid Pontzer, H., 2006. Locomotor Energetics, Ranging Ecology, and the Origin of the 1543 evolution. Am. J. Phys. Anthropol. 129, 499e511. Genus Homo. Doctoral Dissertation, Harvard University. 1597 1544 Geissmann, T., 1986. Estimation of australopithecine stature from long bones A.L. Pontzer, H., 2007a. Limb length and the scaling of locomotor cost in terrestrial 1598 1545 288-1 as a test case. Folia Primatol. 47, 119e127. animals. J. Exp. Biol. 210, 1752e1761. 1599 1546 Griffin, N.L., Richmond, B.G., 2005. Cross-sectional geometry of the human forefoot. Pontzer, H., 2007b. Predicting the cost of locomotion in terrestrial animals: a test of 1600 Bone 37, 253e260. the LiMb model in humans and quadrupeds. J. Exp. Biol. 210, 484e494. 1547 Haeusler, M., McHenry, H.M., 2004. Body proportions of Homo habilis reviewed. J. Pontzer, H., Raichlen, D.A., Sockol, M.D., 2009. The metabolic cost of walking in 1601 1548 Hum. Evol. 46, 433e465. humans, chimpanzees, and early hominins. J. Hum. Evol. 56, 43e54. 1602 1549 Hallgrimsson, B., Willmore, K., Hall, B., 2002. Canalization, developmental stability, and Reikeras, O., Bjerkreim, I., Kolbenstvedt, A., 1983. Anteversion of the acetabulum 1603 1550 morphological integration in primate limbs. Yearbk. Phys. Anthropol. 45, 131e158. and femoral neck in normals and in patients with osteoarthritis of the hip. Acta 1604 Harcourt-Smith, W.E., Aiello, L.C., 2004. Fossils, feet and the evolution of human Orthop. Scand. 54, 18e23. 1551 bipedal locomotion. J. Anat. 204, 403e416. Rightmire, G.P., Lordkipanidze, D., Vekua, A., 2006. Anatomical descriptions, 1605 1552 Hayafune, N., Hayafune, Y., Jacob, H., 1999. Pressure and force distribution charac- comparative studies and evolutionary significance of the hominin skulls from 1606 1553 teristics under the normal foot during the push-off phase in gait. Foot 9, 88e92. Dmanisi, Republic of Georgia. J. Hum. Evol. 50, 115e141. 1607 1554 Hermann, K.L., Egund, N., 1998. Measuring anteversion in the femoral neck from Rittmeister, M., Hanusek, S., Starker, M., 2006. Does tibial rotation correlate with 1608 routine radiographs. Acta Radiol. 39, 410e415. femoral anteversion? Implications for hip arthroplasty. J. Arthroplasty 21, 1555 Hicks, J., Arnol, A., Anderson, F., Schwartz, M., Delp, S., 2007. The effect of excessive 553e558. 1609 1556 tibial torsion on the capacity of muscles to extend the hip and knee during Rolian, C., Lieberman, D.E., Hamill, J., Scott, J.W., Werbel, W., 2009. Walking, running 1610 1557 single-limb stance. Gait Posture 26, 546e552. and the evolution of short toes in humans. J. Exp. Biol. 212, 713e721. 1611 1558 Isbell, L.A., Pruetz, J.D., Lewis, M., Young, T.P., 1998. Locomotor activity difference Ruff, C., 2007. Body size prediction from juvenile skeletal remains. Am. J. Phys. 1612 between sympatric Patas monkeys (Erythrocebus patas) and Vervet monkeys Anthropol. 133, 698e716. 1559 (Cercopithecus aethiops): implications for the evolution of long hindlimb length Ruff, C.B., Trinkaus, E., Holliday, T.W., 1997. Body mass and encephalization in 1613 1560 in Homo. Am. J. Phys. Anthropol. 105, 199e208. Pleistocene Homo. Nature 387, 173e176. 1614 1561 Jungers, W.L., 1982. Lucy’s limbs: skeletal allometry and locomotion in Austral- Ruff, C.B., Walker, A., 1993. Body size and body shape. In: Walker, A., Leakey, R.E. 1615 1562 opithecus afarensis. Nature 297, 676e678. (Eds.), The Nariokotome Homo erectus Skeleton. Harvard University Press, 1616 Jungers, W.L., Harcourt-Smith, W.E.H., Wunderlich, R.E., Tocheri, M.W., Larson, S.G., Cambridge, pp. 234e265. 1563 Sutikna, T., Awe Due, Rhokus, Morwood, M.J., 2009. The foot of Homo flor- Shipman, P., Walker, A., 1989. The costs of becoming a predator. J. Hum. Evol. 18, 1617 1564 esiensis. Nature 459, 81e84. 373e392. 1618 1565 Ker, R.F., Bennett, M.B., Bibby, S.R., Kester, R.C., Alexander, R.McN, 1987. The spring in Simpson, S.W., Quade, J., Levin, N.E., Butler, R., Dupont-Nivet, G., Melanie 1619 1566 the arch of the human foot. Nature 325, 147e149. Everett, M., Semaw, S., 2008. A female Homo erectus pelvis from Gona, Ethiopia. 1620 Klein, R.G., 1999. The Human Career, second ed. Chicago Univ. Press, Chicago. SciencePROOF 322, 1089e1092. 1567 Kram, R., Taylor, C.R., 1990. Energetics of running: a new perspective. Nature 346, Singh, I., 1959. Squatting facets on the talus and tibia in Indians. J. Anat. 93, 1621 1568 265e267. 540e550. 1622 1569 Largey, A., Bonnel, F., Canovas, F., Subsol, G., Chemouny, S., Frédéric Banegas, F., Steudel-Numbers, K., 2006. Energetics in Homo erectus and other early hominins: 1623 1570 2007. Three-dimensional analysis of the intrinsic anatomy of the metatarsal the consequences of increased lower limb length. J. Hum. Evol. 51, 445e453. 1624 bones. J. Foot Ankle Surg. 46, 434e441. Steudel-Numbers, K.L., Tilkens, M.J., 2004. The effect of lower limb length on the 1571 Lejeune, T.M., Willems, P.A., Heglund, N.C., 1998. Mechanics and energetics of energetic cost of locomotion: implications for fossil hominins. J. Hum. Evol. 47, 1625 1572 human locomotion on sand. J. Exp. Biol. 201, 2071e2080. 95e109. 1626 1573 Lewis, O.J., 1980. The joints of the evolving foot. Part III. The fossil evidence. J. Anat. Susman, R.L., de Ruiter, D.J., 2004. New hominin first metatarsal (SK 1813) from 1627 1574 131, 275e298. Swartkrans. J. Hum. Evol. 47, 171e181. 1628 Lieberman, D.E., Raichlen, D.A., Pontzer, H., Bramble, D.M., Cutright-Smith, E., 2006. Susman, R.L., Stern, J.T., 1982. Functional morphology of Homo habilis. Science 217, 1575 The human gluteus maximus muscle and its role in running. J. Exp. Biol. 209, 931e934. 1629 1576 2143e2155. Trinkaus, E., 1981. Neanderthal limb proportions and cold adaptation. In: Stringer, C. 1630 1577 Lordkipanidze, D., Jashashvili, T., Vekua, V., Ponce de Leon, M.S., Zollikofer, C.P.E., B. (Ed.), Aspects of Human Evolution. Taylor and Francis, London, pp. 187e219. 1631 1578 Rightmire, G.P., Pontzer, H., Ferring, R., Oms, O., Tappen, M., Bukhsianidze, M., Vekua, A., Lordkipanidze, D., Rightmire, G.P., Agusti, J., Ferring, R., Maisuradze, G., 1632 Agusti, J., Kahlke, R., Kiladze, G., Martinez-Navarro, B., Mouskhelishvili, A., Mouskhelishvili, A., Nioradze, M., Ponce de Leon, M., Tappen, M., 1579 Nioradze, M., Rook, L., 2007. Postcranial evidence from early Homo from Tvalchrelidze, M., Zollikofer, C., 2002. A new skull of early Homo from Dmanisi, 1633 1580 Dmanisi, Georgia. Nature 449, 305e310. Georgia. Science 297, 85e89. 1634 1581 Lovejoy, C.O., 1999. The natural history of human gait and posture. Part 1. Spine and Walker, A., 1993. Perspectives on the Nariokotome discovery. In: Walker, A., 1635 1582 pelvis. Gait Posture 21, 95e112. Leakey, R.E. (Eds.), The Nariokotome Homo erectus Skeleton. Harvard University 1636 Martin, R., 1957. Lehrbuch der Anthropologie in Systematischer Darstellung mit Press, Cambridge, pp. 411e430. 1583 Besonderer Berücksichtigung der Anthropologischen Methoden. Fischer, Stuttgart. Wallace, I.J., Demes, B., Jungers, W.L., Alvero, M., Sul, A., 2008. The bipedalism of the 1637 1584 McHenry, H., 1992. Body size and proportions in early hominids. Am. J. Phys. Dmanisi hominins: pigeon-toed early Homo? Am. J. Phys. Anthropol. 136, 1638 1585 Anthropol. 87, 407e431. 375e378. 1639 1586 Minetti, A.E., Saibene, F., Ardigo, L.P., Atchou, G., Schena, F., Ferretti, G., 1994. Pygmy Ward, C.V., 2002. Interpreting the posture and locomotion of Australopithecus 1640 locomotion. Eur. J. Appl. Physiol. 68, 285e290. afarensis, where do we stand? Yearbk. Phys. Anthropol. 45, 185e215. 1587 Morton, D.J., 1922. The evolution of the human foot I. Am. J. Phys. Anthropol. 5, Webb, D., 1996. Maximum walking speed and lower limb length in hominids. 1641 1588 305e336. Yearbk. Phys. Anthropol. 101, 515e525. 1642 1589 Myers, M., Steudel, K., 1985. Effect of limb mass distribution on the energetic cost of Wrangham, R.W., Jones, J.H., Laden, G., Pilbeam, D., Conklin-Brittain, N., 1999. The 1643 1590 running. J. Exp. Biol. 16, 363e373. raw and the stolen: cooking and the ecology of human origins. Curr. Anthropol. 1644 Nagel, A., Fernholz, F., Kibele, C., Rosenbaum, D., 2008. Long distance running 40, 567e594. 1591 increases plantar pressures beneath the metatarsal heads-a barefoot walking Young, N.M., Hallgrimsson, B., 2005. Serial homology and the evolution of 1645 1592 investigation of 200 marathon runners. Gait Posture 27, 152e155. mammalian limb covariation structure. Evolution 59, 2691e2704. 1646 1593 O’Connell, J.F., Hawkes, K., Jones, N.G.B., 1999. Grandmothering and the evolution of Yushiok, Y., Siu, D., Cooke, D.V., 1987. The anatomy and functional axes of the femur. 1647 1594 Homo erectus. J. Hum. Evol. 36, 461e485. J. Bone Joint Surg. 69, 873e880. 1648 UNCORRECTED

Please cite this article in press as: Pontzer, H., et al., Locomotor anatomy and biomechanics of the Dmanisi hominins, J Hum Evol (2010), doi:10.1016/j.jhevol.2010.03.006