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Research Article
Postcranial evidence of late Miocene hominin bipedalism in Chad
Franck Guy
Université de Poitiers / CNRS UMR 7262 - PALEVOPRIM Paléontologie, Evolution, Paléo-écosytèmes, Paléoprimatologie
Corresponding Author
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Terrestrial bipedal locomotion is one of the key adaptations defining the hominin clade. Evidences of undisputed bipedalism are known from postcranial remains of late Miocene hominins as soon as 6 Ma in eastern Africa. Bipedality of Sahelanthropus tchadensis was hitherto documented at 7 Ma in central Africa (Chad) by cranial evidence. Here, we present the first postcranial evidence of the locomotor behavior of the Chadian hominin with new insights on bipedalism at the early stage of our evolutionary history. The original material was discovered at locality TM 266 (Toros-Menalla fossiliferous area), and consists in one left femur and two antimeric ulnae. These new findings confirm that hominins were already terrestrial biped relatively soon after the human-chimpanzee divergence but also suggest that careful climbing arboreal behaviors was still a significant part of their locomotor repertoire.
Keywords
Terrestrial bipedal, Miocene hominins, postcranial remains
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Discoveries in Chad by the Mission Paleoanthropological Franco-Tchadienne (MPFT) have substantially contributed to our understanding of early human evolution in Africa. The locality TM 266 (Extended data 1) in the Toros-Menalla fossiliferous area in the Mega-Chad basin yielded, among hundreds of vertebrate remains, a nearly complete cranium (TM 266-01-60-1), three mandibles, and several isolated teeth depicting a minimum of three adult individuals assigned to Sahelanthropus tchadensis1,2. TM 266 fossils were found in the Anthracotheriid Unit with biochronological estimates and radiochronological age at ca. 7 Ma3,4. Environmental indicators at Toros-Menalla localities, at the time, suggested a lacustrine fringe, in a desert vicinity, where open areas with dry and humid grasslands coexisted with arboreal cover5,6.
Three other hominin fossil remains were discovered at TM 266 in 2001 by the MPFT: one left femoral shaft (TM 266-01-063, unearthed in July 2001), and two right and left ulnae (respectively TM 266-01-358, unearthed in November 2001 and TM 266-01-050, unearthed in July 2001; Supplementary notes). Despite none of these limb bones can be reliably ascribed to any hominin craniodental specimen found at TM 266, the most parsimonious hypothesis is that these postcranial remains belong to the sole hominin species present in this locality. Hence, we favor a conservative attribution of these specimens to Sahelanthropus tchadensis.
The hindlimb is documented by a left femoral shaft (TM 266-01-063) of about 242 mm long (Fig. 1 and Supporting table 1, Extended data 2), lacking the distal epiphysis and most of the proximal one. The specimen is curved anteroposteriorly as in Australopithecus7-9 and Orrorin tugenensis (BAR 1002’00 and BAR 1003’00) but more heavily built. The two major mediolateral axes of the proximal and distal diaphyseal portions clearly indicate that the neck must have been anteverted as in fossil hominins9-11 (Extended data 3). The presence of a groove on the postero-superior surface of the neck for the obturator internus and m. gemelli supports this interpretation. Resulting in head/neck torsion relative to the long axis of the shaft12.This condition is also reported in archaic fossil apes such as Nacholapithecus and Ekembo but is absent in the arboreal biped Danuvius13. The femur exhibits proximal platymeria just distal to the lesser trochanter (Supplementary notes), a trait encountered in O. tugenensis and later hominins and suggested to correlate with neck elongation, a reliable indicator of hominin bipedalism9,14-16 (but see 8,17). Concurrently, the neck is compressed antero-posteriorly as in the Miocene ape Danuvius guggenmosi13 and hominins8-9,18 (but see 19 for Dryopithecus fontani and Hispanopithecus laietanus; Fig. 1). This array of features agrees with habitual bipedalism in S. tchadensis.
A small but sharp relief, indicative of the third trochanter, continues into a rugose surface distally and blends with the lateral component of a broad ‘proto-linea aspera’17 (12.2mm in its narrowest width). The lateral lip of the linea forms a well-marked sigmoid line. Similarly, the medial lip of the linea aspera is well-marked. The spiral line for the insertion of the vastus medialis consists in a straight line, which confounds distally with the medial lip of the linea aspera. Such configuration is also observed in O. tugenensis and Ardipithecus ramidus8,16,18 albeit with a more salient ‘proto-linea aspera’ in TM 266-01-063, but differs from modern humans where a pilaster develops. Such an overall pattern is consistent with bipedalism albeit suggesting a less-developed quadriceps system relative to the hamstring compared to modern human-like pattern17.
The femoral shaft exhibits thick cortical bone in cross-section (Fig. 2). Cortical thickness distribution pattern describes a posterior and lateral thickening of the diaphysis relative to an anterior and medial thinning (Fig. 3). Posterior thickening of the cortical bone occurs at the level of the nutrient foramen, where the ‘proto-linea aspera’ is the narrowest. Conversely, extant apes share a posterior thickening on proximal half of the shaft and a relative thinning on distal half20 (see also Supporting Information in 21). Lateral thickening can be traced on the major part of the shaft in TM 266-01-063 except in its most distal portion. African apes do not display extended lateral thickening but instead, a circumscribed thickening corresponding to the lateral spiral pilaster. In these aspects, TM 266-01-063 most resembles extant humans. Comparative data are, to our knowledge, inexistent for Ardipithecus. Besides, cortical thickness data reported for BAR 1002’00 (O. tugenensis) rely on CT-scan data whose reliability is questionable22-24.
Cortical area and second moment of area (Ix/Iy and Imax/Imin are biomechanical parameters frequently used to infer habitual locomotor functions in primates, as they reflect loads undergone by long bones during growth (but see 25). The cortical area of the diaphyseal cross-section is a measure of resistance of the bone to axial compression or tension, while second moment of area measures the resistance to bending loads. In TM 266-01-063, percent of cortical area is 66.5 % at the level of the nutrient foramen (see Methods) and slightly increase proximally. It is within the range of extant and fossil apes (75 % ± 3.6 in extant humans; 63.3 % ± 7.6 in chimpanzees; 70 % ± 3.9 in gorillas; Supporting Information in 21) and above the value reported for AL 288-1 femur (59.9 %) at midshaft26. Response to bending loads endured by the femur from TM 266 is assessed at the level of the nutrient foramen using second moment of area26,27. Results for Imax/Imin and Ix/Iy are respectively 1.31 and 0.81 (Extended data 4). The Chadian femur approaches the chimpanzee/extant human condition in its Imax/Imin ratio (measured at midshaft28,29; humans, Imax/Imin=1.6 ± 0.36; chimpanzees, Imax/Imin=1.4 ± 0.2) whereas it departs from gorillas28 (Imax/Imin=1.9 ± 0.3). The Ix/Iy of TM 266-01-063 is close to values reported for chimpanzees (chimpanzee30: Ix/Iy=0.75 ± 0.08), early Homo31-33 and early to Middle Pleistocene hominins34. It departs from extant humans in which a posterior pilaster develops29 (Ix/Iy =1.52 ± 0.39). Whereas midshaft cross-section of TM 266-01-063 resembles in its overall aspect to AL 288-1, the Chadian specimen present higher Imax/Imin and lower Ix/Iy values than its younger eastern-African relative (A. afarensis: AL 288-126, Ix/Iy=0.98 and Imax/Imin=1.07; see also 35 for AL 333-61, Ix/Iy=1.16 and Imax/Imin=1.16).
Many aspects such as stature, body mass, muscle attachment sites, positional behavior, ontogeny and sexual dimorphism25 may contribute to femoral bone mass distribution. Yet, geometry of the TM 266-01-063 indicates greatest bending resistance for medio-laterally oriented stresses. This condition seen in AL 288-1 and early African and Asian Homo is suggested to relate to a more lateral position of the body during the stance phase of gait in association with an increase in femoral neck length and biacetabular breadth26. Functional interpretations remain difficult to formulate given the paucity of early hominin comparative data and given the state of preservation of the Chadian femur. Nevertheless, the Chadian femoral shaft exhibits a well-developed calcar femorale (CF) in its proximal portion (Fig. 4; the CF is 18.80 mm long measured at the level of the lesser trochanter following36), a condition to date only seen in extant humans and reported in O. tugenensis (BAR 1003’00). The calcar femorale corresponds to a bony wall that originates from the postero-medial endosteal surface at the level of the lesser trochanter and extends laterally toward the greater trochanter. In obligate bipeds, it facilitates compressive loads dispelling in the proximal femur by decreasing the stress in the posterior and medial aspects and increasing the stress in the anterior and lateral aspects36,37. A well-developed calcar femorale in TM 266-01-063 represents a morphological requirement for terrestrial bipedalism.
The forearm bones attributed to Sahelanthropus tchadensis consist in two partial left and right ulnae lacking the distal epiphyses. Similarity in size and shape for the antimeric ulnae could suggest they are from the same individual, even if no definitive evidence supports this assumption. TM 266-01-050 is a left ulnar diaphysis of 239 mm long (Fig. 5, Supporting table 1, Extended data 2) showing eroded proximal epiphysis. The right ulna (TM 266-01-358) corresponds to a proximal-half shaft of 155 mm long with partially preserved epiphysis. The shafts are curved in profile. Similar anteroposterior curvature is observed in Ar. kadabba38 (ALA-VP 2/101) and later hominins StW 573k and OH 36, as in extant apes9,39,40. This feature contrasts with the straight right ulnar shafts of D. guggenmosi and A. prometheus, but this lack of curvature is likely due to a pathological condition9,13. In primates, such ulnar curvature is due to habitual loads exerted by the action of m. brachialis in order to maintain elbow flexion in arboreal context, which in turn involves the antagonistic action of a powerful forearm musculature, including wrist and fingers extensors and flexors40,41.
The preserved flat distal portion of the olecranons indicate that they were not projecting posteriorly as in extant African apes42. In this regard, the distal portion of the olecranon most resembles the condition seen in Miocene apes42-44 and in hominins42. The proximal epiphyses indicates an anteriorly-facing trochlear notch as in fossil hominins and Miocene apes9,13,42-45. Hence, the Toros-Menalla ulnae depart from the typical proximally oriented trochlear notch in extant great apes41,46. In functional terms, a more anteriorly facing notch, associated with an olecranon aligned with the long axis of the forearm, favors triceps leverage at mid-flexion41,46. In Ar. ramidus such function is linked to careful climbing and bridging44. Conversely, a more proximally facing notch reflects differential loading during suspension43 while a posteriorly projecting olecranon favors triceps leverage in extension and is commonly associated with terrestrial quadrupedal locomotion in anthropoids42.
Ulnae from Toros-Menalla display a keeled trochlear notch with a comparatively acute angle relative to later hominins and African apes. The distal keeling angle, measured from TM 266-01-358 (distal keeling angle=109°), is in the lower range of Pongo pygmaeus and close to the value reported for Oreopithecus bambolii and the left ulna AL 288-1t in A. afarensis46. Likewise, the proximal angle is acute (proximal keeling angle=100°), in the lower range of reported values for chimpanzees, and close to OH 36 and Or. bambolii46. A pronounced trochlear keel warrants medio-lateral stability of the elbow in response to powerful superficial finger and wrist flexors, and forearm pronator (mm flexor digitorum superficialis, flexor carpi radialis and ulnaris, and pronator teres)39,46. Such configuration was supposedly reported on D. guggenmosi13 and is typical of the arboreal large apes, which integrates climbing, and/or suspension in their locomotor repertoire46. It is unlikely to reflect habitual terrestrial quadrupedalism. The TM 266 ulnae lack prominent flexor apparatus entheses as in orangutans, Ar. ramidus and later hominins. In this respect, it differs from the condition seen in Miocene apes and extant quadrupedal monkeys. Such morphology precludes the possibility of quadrupedalism and, more specifically, of knuckle-walking as primary locomotor behaviors for the Toros-Menalla hominins45.
Overall, the trochlear notch of TM 266 ulnae present an unusual morphology as the middle portion is mediolaterally narrow relative to the distal half. This waisted aspect of the trochlear notch approaches the condition seen in ‘small’ apes (humans, chimpanzees and bonobos) and contrasts with that of ‘large’ apes (orangutans and gorillas). Such configuration is interpreted as locomotor-independent and rather linked to allometry46. The disto-medial quadrant of TM 266-01-358 is clearly more developed than the distolateral one, an intermediate morphology between humans and chimpanzees, close to that of D. guggenmosi13, A. afarensis, and A. prometheus 9,46. A developed medial portion of the trochlear notch is an adaptation for maximum joint compression medially, a configuration which could meet mechanical requirements in various non terrestrial locomotor behaviors13,46.
Only limited portions, proximally and distally, of TM 266-01-050 allow assessing cortical bone distribution (see Supplementary notes, Extended data 4). Proximally, the percent of cortical area is 73.4 %, measured at about 70-75 % of the estimated total lengths of the ulna (see methods). At mid-shaft, the percent of cortical area is 81.0 %, falling within the variation of Late Pleistocene hominins (80.1 % ± 6.6 in H. sapiens and 82.8 % ± 7.1 in neandertals)47. Besides, Imax/Imin and Ix/Iy are respectively 2.04/1.62 at 70-75 % level and 1.71/1.13 at midshaft. Values for the Chadian ulna fall outside the reported variation for gorillas48 and is within the range of variation in chimpanzees for proximal Imax/Imin and proximal-midshaft Ix/Iy. Besides, TM 266-01-050 is within the range of variation of Asian non-human apes for all ratios except for the lower measured proximal Imax/Imin in Pongo. The geometry of TM 266-01-050 deviates from circularity in the antero-posterior direction. The cortical bone is predominantly distributed antero-posteriorly as in orangutans and to a lesser extent in chimpanzees. This condition contrasts with the one seen in gorillas, which tend to grow more bone medio-laterally. Relative medio-lateral expansion is suggested to adjust for increased vertical and medio-lateral forces that apply to the forelimb in terrestrial quadrupedal primates45,49,50. Besides, considering comparative data available for chimpanzees and orangutans, which tend to grow more bone antero-posteriorly51, the Chadian ulna configuration more likely reflects bending loads associated with a wide array of arboreal locomotor modes. Yet, the TM forelimb bones lack any traits typical of suspension or knuckle walking, and exhibit a configuration better seen in apes engaged in careful climbing44. However, the possibility that the Chadian hominin was capable of vertical climbing cannot be dismissed given the particularly keeled trochlear notch.
The Toros-Menalla femur exhibits several hallmarks of habitual terrestrial bipedalism. Among them, a well-defined broad proto-linea aspera, the presence of a lateral third trochanter and associated subtrochanteric platymeria without hypotrochanteric or infero-lateral fossae, is classically associated with enhanced hip flexion-extension16,20,52, while a particularly developed calcar femorale facilitates compressive loads dispelling in terrestrial bipedalism36. These features go with an overall cortical bone distribution pattern and cross-section geometries of the femoral shaft that suggest muscular recruitments and bone loads compatibles with habitual bipedalism. Despite some of the above-mentioned traits are suggested to be the primitive condition in hominins (proximal platymeria or gluteal tuberosity)17, they are part of a functional complex co-opted for bipedalism. They are routinely considered as such to infer potential bipedal terrestrial locomotion in early eastern African hominins7,8,16,18,52,53. The Chadian hindlimb bone conforms to the overall morphological pattern of Miocene hominin terrestrial bipeds. The forelimbs morphology rules out arboreal specialization for the Chadian material, as in Ar. ramidus16 and presumably O. tugenensis7. Yet, the Chadian postcranial material displays a suite of morphological features that are consistent with substantial non-stereotypical arboreal behaviors, as suggested by ulnar shaft curvature and cross-section geometrical properties, whereas the elbow morphology is potentially indicative of careful climbing44, and does not display any evidence of knuckle-walking.
Recently, it was suggested that the putative stem hominid D. guggenmosi was able to use obligate arboreal bipedalism combined to suspension as early as the late middle Miocene13. The authors suggested that hominin terrestrial bipedalism and great ape suspension evolved from such locomotor repertoire13. In the lack of evidence supporting a phylogenetic relationship between hominins and Miocene European apes, we cannot infer that hominin terrestrial bipedalism originated from middle Miocene forms in Europe as suggested by 13. Instead, the Chadian remains described herein reassert African roots. They are the first direct evidence of an obligate terrestrial bipedalism, indistinguishable from that inferred for O. tugenensis and Ar. kadabba/ramidus. They suggest a precocious adaptation to bipedalism after the human-chimp dichotomy54. The Chadian remains suggests a conservative evolution of climbing capacities, interpreted as cautious climbing as in stem apes54. Hence, cautious climbing modality weakens a potential role of suspension in the emergence of the hominin clade13.
The Toros-Menalla postcranial material also reasserts the presence of cladistic hominins in the upper Miocene of Chad, within particular environmental settings. Eastern African Miocene hominins are associated with open woodland areas with significant tree cover at ~6 Ma at Lukeino55, and a mixture of woodland combined with wet grassland for the earliest postcranial-based bipedalism occurrence in Ethiopia at 5.2 Ma (AME-VP-1/71, Ardipithecus kadabba)38,56. At 4.4 Ma, Ar. ramidus most probably inhabited a ground-water-fed grassy woodland (probably a palm grove) at Aramis57-58.
Taken as a whole, eastern-African early hominins share an arboreal component in their habitat (see 57,59 for discussion on Aramis). Environmental indicators in Toros-Menalla fossiliferous area suggest heterogeneous landscape types consisting of closed forest formations (probably riparian forests), palm grove formations, and mixed/grassland formations (from woodlands to savannas/aquatic grasslands)5,6,60. Therefore, the Chadian hominins were probably no exception as being reliant on arboreal cover given their potential climbing abilities. As bipeds, they were not exclusive arboreal forest dwellers, because they were able to raid in near open environments for food/water resource harvesting. The association between a polyvalent locomotion (arboreality and bipedal terrestriality), and wooded formations in mesic context during at least ~2.5 million years suggests that the ecological niche of these early hominins was not strongly tied to the expansion of relatively dry, open areas. This niche could be depicted as opportunistic in its reliance on both terrestrial and arboreal resources.
Based on molecular data, the chimpanzee-human last common ancestor (CHCLA) is estimated to occur in Africa between 10 and 7 Ma61,62. Indeed, fossil representatives of the panin clade are too scarce and consists in a minimum of three Middle Pleistocene teeth from the Kapthurin formation in Kenya63 and a chimpanzee-like proximal femoral epiphysis of unknown age from the Kikorongo crater in Uganda64. However, at least three taxa have been described between 10 Ma and 7 Ma in African deposits: Samburupithecus, from Samburu Hills, around 9.5 Ma65, Nakalipithecus from Nakali, around 9,8 Ma66 and Chororapithecus from the Middle Awash, around 8 Ma62,67. These Miocene taxa are parsimoniously assigned to stem hominines68,69, even if Samburupithecus displays a particularly archaic morphology69. Chororapithecus displays derived dental affinities with Gorilla67. In light of this record and of the lack of phylogenetic resolution, the ancestral condition of positional behaviour in African apes and humans will remain elusive until significant new data becomes available. To date, the identification of the derived traits shared by hominins relies on the analysis of the earliest forms of the clade. The early hominins Sahelanthropus, Orrorin and Ardipithecus share the same combination of non-honing C-P3 complex and of features linked to terrestrial bipedalism. This combination is arguably more similar to the condition observed in later hominins than in any other African fossil or extant hominoids. This is currently the only data available for formulating scenarios about the latest Miocene/earliest Pliocene evolution of African hominoids. In absence of Mio-Pliocene fossils displaying exclusive morphological affinities with Pan, cautionary tales about rampant homoplasy and character polarity in this evolutionary sequence70 are poorly suitable to falsification attempts. Instead, the morphological homogeneity of the purported hominids implies that the interpretation of the combined non-honing C-P3 complex-bipedal hindlimb as a synapomorphic signature of early hominids currently remains the most parsimonious hypothesis
The original fossil specimens are measured to the nearest 0.1 mm using a Mitutoyo sliding digital caliper.
Computed tomography
High-resolution micro-computed tomography (HR-mCT) images taken from the original femur and ulnae were used to assess the inner morphology of the bones. The material was scanned with EasyTom XL Duo mCT (using a sealed Hamamatsu microfocus x-ray source - 75 W, 150 kV - and an amorphous silicon based detector Varian PaxScan 2520DX, 1536*1920 pixel matrix; 127 mm pixel pitch, 16 bits, CsI conversion screen - from RX-Solutions, France) at Plateforme PLATINA (University of Poitiers). For scanning procedures, beam intensity was set at 90 kV and tube current at 333 mA. The TM 266- 01-358 ulna was acquired with 3584 projections resulting in 3036 slices of 730*825 pixels using a cone-beam reconstruction algorithm. The isovoxel size was set to 0.0525 mm. The TM 266-01-050 ulna was acquired with 4800 projections resulting in 4051 slices of 589*849 pixels. The isovoxel size was set to 0.0600 mm. The TM 266-01-063 femur was acquired with 5984 projections resulting in 4962 slices of 1162*911 pixels. The isovoxel size was set to 0.0499 mm.
Virtual models processing
Semi-automatic segmentation of the virtual fossil specimens and three-dimensional surfaces extraction were performed in Avizo Lite. Three-dimensional surfaces were prepared and treated using Geomagic Studio. Cortical bone thickness distribution was assessed in three dimensions using the Surface thickness module in Avizo Lite from the outer surface of the of the segmented medullar cavity to the outer surface of the femur. All measurements based on 3D virtual models of the fossil specimen were done in Avizo Lite on 3D volumes and Fiji image software71 on 2D slices.
Cross-sectional geometric properties (CSGP)
The femur lacks the most part of the epiphyses, which prevents from estimating its biomechanical length. However, CSGP values in Homo and Pan do no show significant differences between 45-55 % of the femoral (biomechanical or maximum) length31. Comparison of diaphyseal cross-sectional geometry from fragmentary specimens must be evaluated on a case-by-case basis31. Superimposition of the femora BAR 1002'00 (O. tugenensis) and TM 266-01-063 using the distal base of their lesser trochanter (corresponding to 80 % of the biomechanical length72), show that the nutrient foramen on TM 266-01-063 provides a reliable indicator of the midshaft level. CSGP estimates were computed at nutrient foramen level and then, in order to get an assessment of the variation pattern of cortical bone distribution, at four additional cross-sections, equally spaced from the nutrient foramen to the base of the lesser trochanter. For ulnae, CSGP variables were computed proximally from 35.0 mm below the distal border of the radial notch (and at the level of the nutrient foramen), which corresponds to 70-75 % of the estimated ulna length for TM 266-01-050 (estimated using OMO L40-19 fossil hominin ulna as analog).
Percentage of cortical area and second moment of area were computed using Fiji image software71 and BoneJ plugin73.
Comparative data for CSGP with extant and extinct hominoids (Extended data 4) were gathered from 19,21,26,28-30,32,33,35,74,75.
- Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nature methods 9, 676-682 (2012).
- Ruff, C. B. Long bone articular and diaphyseal structure in Old World monkeys and apes. I: locomotor effects. Am. J. Phys. Anthrop. 119, 305-342 (2002)
- 73. Doube, M. et al. BoneJ: Free and extensible bone image analysis in ImageJ. Bone 47, 1076-1079 (2010).
- MaClatchy, L., Gebo, D., Kityo, R., & Pilbeam, D. Postcranial functional morphology of Morotopithecus bishopi, with implications for the evolution of modern ape locomotion. J. Hum. Evol. 39, 159-183 (2000).
- Rodríguez, L., Carretero, J. M., García-González, R., & Arsuaga, J. L. Cross-sectional properties of the lower limb long bones in the Middle Pleistocene Sima de los Huesos sample (Sierra de Atapuerca, Spain). J. Hum. Evol. 117, 1-12 (2018).
Author contributions
G.D. and F. G. designed the study, collected and interpreted the data. G.D., F.G. and J.-R. B. wrote the manuscript. G. D., F. G., J.-R. B., M.H.T., A.L., M.A., P.V. and C.N. discussed the results and revised earlier drafts of the papers.
Acknowledgments
We thank the Chadian Authorities (Ministère de l’Education Nationale de l’Enseignement Supérieur, de la Recherche et de l’Innovation, Université de Djamena & CNRD). We extend gratitude for their support to the French Ministries, Ministère Français de l’Education Nationale (Collège de France, Université de Poitiers), Ministère de la Recherche (CNRS), Ministère de l’Europe et des affaires étrangères (Direction de la Coopération Scientifique, Universitaire et de Recherche, Paris, and SCAC Ambassade de France à N’djamena, Commission de Consultation des recherches Archéologiques à l'Etranger), to the Région Nouvelle Aquitaine, and also to the Armée Française (MAM, Epervier and Barkhane) for logistic support. We would like to thank deeply to Professor M. Brunet, head of the M.P.F.T., who initiated this work and gathered the first comparative data at the basis of the present manuscript. For giving him the opportunity to work with their collections, we are grateful to our Colleagues and their Institutions: C.O. Lovejoy (Kent State University), B. Asfaw (National Museum of Ethiopia), Y. Haile-Selassie (Cleveland Museum of Natural History), M. G. Leakey & R. Leakey (National Museum of Kenya), D. Pilbeam (Peabody Museum and Harvard University), D. Johanson & W. Kimbel (Institute of Human Origins and Arizona State University at Tempe), T. White (University of California at Berkeley) and G. Suwa (University Museum of Tokyo). Special thanks to all our colleagues and friends for their help and discussion, and particularly to D. Barboni, A. Mazurier (Centre de Microtomographie), A. Novello. We especially thank all the MPFT members who participated to the field missions, and Ahounta D., Fanoné G. (deceased), Mahamat A., S. Riffaut, J. Surault and X. Valentin for technical support. We are most grateful to G. Florent, C. Noël, G. Reynaud, C. Baron, M. Pourade, and L. Painault for administrative guidance.
- Brunet, M. et al. A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418, 145–151 (2002).
- Brunet, M. et al. New material of the earliest hominid from the Upper Miocene of Chad. Nature 434, 752–755 (2005).
- Vignaud, P. et al. Geology and palaeontology of the Upper Miocene Toros-Menalla hominid locality, Chad. Nature 418, 152–155 (2002).
- Lebatard, A. E. et al. Cosmogenic nuclide dating of Sahelanthropus tchadensis and Australopithecus bahrelghazali: Mio-Pliocene hominids from Chad. Proc. Natl. Acad. Sci. USA 105, 3226–3231 (2008).
- Le Fur, S., Fara, E., Mackaye, H. T., Vignaud, P., & Brunet, M. The mammal assemblage of the hominid site TM266 (Late Miocene, Chad Basin): ecological structure and paleoenvironmental implications. Naturwissenschaften 96, 565–574 (2009).
- Schuster, M. et al. Chad Basin: paleoenvironments of the Sahara since the Late Miocene. C. R. Geosci. 341, 603–611 (2009).
- Senut, B. et al. First hominid from the Miocene (Lukeino formation, Kenya). C. R. Acad. Sci. Paris IIA 332, 137–144 (2001).
- Pickford, M., Senut, B., Gommery, D., & Treil, J. Bipedalism in Orrorin tugenensis revealed by its femora. C. R. Palevol 1, 191–203 (2002).
- Heaton, J. L. et al. The long limb bones of the StW 573 Australopithecus skeleton from Sterkfontein Member 2: Descriptions and proportions. J. Hum. Evol. 133, 167–197 (2019).
- Lovejoy, C. O., Cohn, M. J., & White, T. D. Morphological analysis of the mammalian postcranium: a developmental perspective. PNAS, 96, 13247–13252 (1999).
- Tardieu, C. Development of the human hind limb and its importance for the evolution of bipedalism. Evol Anthrop: Issues, News, and Reviews, 19, 174–186 (2010).
- Marchi, D. et al. The thigh and leg of Homo naledi. J. Hum. Evol. 104, 174–204 (2017).
- Böhme, M. et al. A new Miocene ape and locomotion in the ancestor of great apes and humans. Nature, 575, 489–493 (2019).
- Ruff, C. in Primate Locomotion: Recent Advances (eds. Strasser, E., Fleagle, J., Rosenberger, A.L., & McHenry, H.) 449–469 (Springer, Boston, MA, 1998).
- Lovejoy, C. O., Meindl, R. S., Ohman, J. C., Heiple, K. G., & White, T. D. The Maka femur and its bearing on the antiquity of human walking: applying contemporary concepts of morphogenesis to the human fossil record. Am. J. Phys. Anthropol. 119, 97–133 (2002).
- Lovejoy, C. O., Suwa, G., Spurlock, L., Asfaw, B., & White, T. D. The pelvis and femur of Ardipithecus ramidus: the emergence of upright walking. Science 326, 71e1-71e6 (2009).
- Almécija, S. et al. The femur of Orrorin tugenensis exhibits morphometric affinities with both Miocene apes and later hominins. Nat. Commun. 4, 2888 (2013).
- Richmond, B. G., & Jungers, W. L. Orrorin tugenensis femoral morphology and the evolution of hominin bipedalism. Science 319, 1662–1665 (2008).
- Pina, M. Unravelling the positional behaviour of fossil hominoids morphofunctional and structural analysis of the primate hindlimb. Doctoral dissertation, Universitat Autònoma de Barcelona (2016).
- Morimoto, N., De León, M. S. P., Nishimura, T., & Zollikofer, C. P. Femoral morphology and femoropelvic musculoskeletal anatomy of humans and great apes: a comparative virtopsy study. Anat. Rec. 294, 1433–1445 (2011).
- Macchiarelli, R. & Zanolli, C. Hominin biomechanics, virtual anatomy and inner structural morphology: From head to toe. A tribute to Laurent Puymerail. C. R. Palevol 16, 493–498 (2017).
- Eckhardt, R. B., Galik, G., & Kuperavage, A. J. Questions about Orrorin femur: response. Science 307, 845 (2005).
- Galik, K. et al. External and internal morphology of the BAR 1002'00 Orrorin tugenensis femur. Science 305, 1450–1453 (2004).
- Ohman, J. C., Lovejoy, C. O., & White, T. D. Questions about Orrorin femur. Science 307, 845 (2005).
- Lieberman, D. E., Polk, J. D., & Demes, B. Predicting long bone loading from cross-sectional geometry. Am. J. Phys. Anthropol. 123, 156–171 (2004).
- Ruff, C. B., Burgess, M. L., Ketcham, R. A., & Kappelman, J. Limb Bone Structural Proportions and Locomotor Behavior in AL 288-1 (" Lucy"). PLoS ONE 11, e0166095 (2016).
- Lovejoy, C. O., Burstein, A. H., & Heiple, K. G. The biomechanical analysis of bone strength: a method and its application to platycnemia. Am. J. Phys. Anthropol. 44, 489–505 (1976).
- Mongle, C. S., Wallace, I. J. & Grine, F. E. Cross-sectional structural variation relative to midshaft along hominine diaphyses. II. The hind limb. Am. J. Phys. Anthropol. 158, 398–407 (2015).
- Trinkaus, E. & Ruff, C. B. Femoral and Tibial Diaphyseal Cross-Sectional Geometry in Pleistocene Homo. PaleoAnthropology 2012, 13–62 (2012).
- Nadell, J. Ontogeny and Adaptation: A Cross-Sectional Study of Primate Limb Elements. Doctoral dissertation, Durham University (2017).
- Puymerail, L. et al. Structural analysis of the Kresna 11 Homo erectus femoral shaft (Sangiran, Java). J. Hum. Evol. 63, 741–749 (2012).
- Ruff, C. Femoral/humeral strength in early African Homo erectus. J. Hum. Evol. 54, 383–390 (2008).
- Ruff, C. Relative limb strength and locomotion in Homo habilis. Am. J. Phys. Anthropol. 138, 90–100 (2009).
- Ruff, C. B., Puymerail, L., Macchiarelli, R., Sipla, J., & Ciochon, R. L. Structure and composition of the Trinil femora: functional and taxonomic implications. J. Hum. Evol. 80, 147–158 (2015).
- Chevalier, T. AL 333 – 61 femoral diaphysis: evidence of obligate bipedalism 3.2 million years ago in Ethiopia? Bull. Mém. Soc. Anthropol. Paris 25:169–189 (2013).
- Kuperavage, A., Pokrajac, D., Chavanaves, S. & Eckhardt, R. B. Earliest known hominin calcar femorale in Orrorin tugenensis provides further internal anatomical evidence for origin of human bipedal locomotion. Anat. Rec. 301, 1834–1839 (2018).
- Zhang, Q. et al. The role of the calcar femorale in stress distribution in the proximal femur. Orthop. surg., 1, 311–316 (2009).
- Haile-Selassie, Y., Suwa, G. & White, T. in Ardipithecus kadabba: Late Miocene Evidence From The Middle Awash, Ethiopia (eds. Haile-Selassie, Y., & WoldeGabriel, G.) 159–236 (Univ of California Press, 2009).
- Drapeau, M. S. M., Ward, C. V., Kimbel, W. H., Johanson, D. C., & Rak, Y. Associated cranial and forelimb remains attributed to Australopithecus afarensis from Hadar, Ethiopia. J. Hum. Evol. 48, 593–642 (2005).
- Henderson, K., Pantinople, J., McCabe, K., Richards, H. L. & Milne, N. Forelimb bone curvature in terrestrial and arboreal mammals. PeerJ 5, e3229 (2017).
- Drapeau, M. S. M. Functional anatomy of the olecranon process in hominoids and Plio-Pleistocene hominins. Am. J. Phys. Anthropol. 124, 297–314 (2004).
- Begun, D. R. Phyletic diversity and locomotion in primitive European hominids. Am. J. Phys. Anthropol. 87, 311–340 (1992).
- Takano, T. et al. Forelimb long bones of Nacholapithecus (KNM-BG 35250) from the middle Miocene in Nachola, northern Kenya. Anthropol. Sci. 126, 135–149 (2018).
- Lovejoy, C. O., Simpson, S. W., White, T. D., Asfaw, B., & Suwa, G. Careful climbing in the Miocene: the forelimbs of Ardipithecus ramidus and humans are primitive. Science 326, 70e1-70e8 (2009).
- Alba, D. M., Almécija, S., Casanovas-Vilar, I., Méndez, J. M., & Moyà-Solà, S. A partial skeleton of the fossil great ape Hispanopithecus laietanus from Can Feu and the mosaic evolution of crown-hominoid positional behaviors. PLoS ONE 7, e39617 (2012).
- Drapeau, M. S. M. Articular morphology of the proximal ulna in extant and fossil hominoids and hominins. J. Hum. Evol. 55, 86–102 (2008).
- Churchill, S. E. et al. Morphological affinities of the proximal ulna from Klasies River main site: archaic or modern? J. Hum. Evol. 31, 213–237 (1996).
- Nadell, J.A. Ontogeny and adaptation: a cross-sectional study of primate limb elements, Doctoral dissertation, Durham University (2017).
- Carlson, K.J. et al. Role of nonbehavioral factors in adjusting long bone diaphyseal structure in free-ranging Pan troglodytes. Int. J. Primatol. 29, 1401–1420 (2008).
- Schmitt, D. Mediolateral reaction forces and forelimb anatomy in quadrupedal primates: implications for interpreting locomotor behavior in fossil primates. J. Hum. Evol. 44, 47–58 (2003).
- Morimoto, N. et al. Let bone and muscle talk together: a study of real and virtual dissection and its implications for femoral musculoskeletal structure of chimpanzees. J. Anat. 226, 258–267 (2015).
- White, T. D. et al. Asa Issie, Aramis and the origin of Australopithecus. Nature 440, 883–889 (2006).
- Ward, C. V., Kimbel, W. H., Harmon, E. H. & Johanson, D. C. New postcranial fossils of Australopithecus afarensis from Hadar, Ethiopia (1990–2007). J. Hum. Evol. 63, 1–51 (2012).
- Lovejoy, C. O. et al. The great divides: Ardipithecus ramidus reveals the postcrania of our last common ancestors with African apes. Science 326, 73–106 (2009).
- Bamford, M. K., Senut, B. & Pickford, M. Fossil leaves from Lukeino, a 6-million-year-old Formation in the Baringo Basin, Kenya. Geobios 46, 253–272 (2013).
- WoldeGabriel, G. et al. Geology and palaeontology of the late Miocene Middle Awash valley, Afar rift, Ethiopia. Nature 412, 175–178 (2001).
- White, T. D. et al. Macrovertebrate paleontology and the Pliocene habitat of Ardipithecus ramidus. Science 326, 67–93 (2009).
- Barboni, D., Ashley, G. M., Bourel, B., Arraiz, H. & Mazur, J. C. Springs, palm groves, and the record of early hominins in Africa. Rev. Palaeobot. Palynol. 266, 23–41 (2019).
- Cerling, T. E. et al. Woody cover and hominin environments in the past 6 million years. Nature 476, 51–56 (2011).
- Novello, A. et al. Phytoliths indicate significant arboreal cover at Sahelanthropus type locality TM266 in northern Chad and a decrease in later sites. J. Hum. Evol. 106, 66–83 (2017).
- Steiper, M. E. & Young, N. M. Timing primate evolution: lessons from the discordance between molecular and paleontological estimates. Evol. Anthropol. 17, 179–188 (2008).
- Katoh, S. et al. New geological and palaeontological age constraint for the gorilla–human lineage split. Nature 530, 215–218 (2016).
- McBrearty, S. & Jablonski, N. G. First fossil chimpanzee. Nature 437, 105–108 (2005).
- DeSilva, J., Shoreman, E. & MacLatchy, L. A fossil hominoid proximal femur from Kikorongo Crater, southwestern Uganda. J. Hum. Evol. 50, 687–695 (2006).
- Ishida H. & Pickford M. A new late Miocene hominoid from Kenya: Samburupithecus kiptalami gen. et sp. nov. C.R. Acad. Sci. Paris 325,823–829 (1997).
- Kunimatsu, Y. et al. A new Late Miocene great ape from Kenya and its implications for the origins of African great apes and humans. Proc. Natl Acad. Sci. USA 104, 19220–19225 (2007).
- Suwa G., Kono R.T., Katoh S., Asfaw B. & Beyene Y. A new species of great ape from the late Miocene epoch in Ethiopia. Nature 448, 921–924 (2007).
- Harrison, T. in Cenozoic Mammals of Africa (eds. Werdelin, L. & Sanders,W.J.) 429–469 (Univ of California Press, Berkeley, 2010).
- Begun, D.R. in Handbook of Paleoanthropology, (eds. Henke, W. & Tattersall, I.) 1261–1332 (Springer-Verlag, Berlin Heidelberg, 2015)
- Wood, B. & Harrison, T. The evolutionary context of the first hominins. Nature 470: 347–352 (2011).
This is a list of supplementary files associated with this preprint. Click to download.
- ExtData1.tif
Extended Data 1: Schematic Map of the Republic of Chad and localization of TM 266 locality.
- ExtData2.tif
Extended Data 2: . Illustration of the postcranial original material from Toros-Menalla, Chad. TM 266-01-063 femur: a, anterior view; b, posterior view; c, lateral view; d, medial view. TM 266-01-358 ulna: e, anterior view; f, posterior view; g, lateral view; h, medial view. TM 266- 01-050 ulna: i, anterior view; j, posterior view; k, lateral view; l, medial view.
- ExtData3.tif
Extended Data 3: Illustration and estimation of the femoral anteversion. a. view of the femur showing proximal plan; b view of the femur showing the distal plan; c, micro-CT slice showing the major axis of the diaphyseal proximal cross section; d, micro-CT slice showing the major axis of the diaphyseal distal cross section; e, superimposition of the medial and distal axes forming an angle of about 26°.
- ExtData4.tif
Extended Data 4: Comparative CSGP data for TM 266 femur and ulnae. Comparisons of the TM 266-01-50 ulna and extant hominoid values for a, Imax/Imin and b, Ix/Iy. Comparisons of the TM 266-01-063 femur and extant hominoid values for c, Imax/Imin; d, Ix/Iy and e, %CA (see methods). Circles are for means and whiskers for standard deviations.
- Supplementarynotes.docx
Supplementary Information
- SupplementaryTable1.xlsx
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Research Article
Postcranial evidence of late Miocene hominin bipedalism in Chad
Franck Guy
Université de Poitiers / CNRS UMR 7262 - PALEVOPRIM Paléontologie, Evolution, Paléo-écosytèmes, Paléoprimatologie
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Terrestrial bipedal locomotion is one of the key adaptations defining the hominin clade. Evidences of undisputed bipedalism are known from postcranial remains of late Miocene hominins as soon as 6 Ma in eastern Africa. Bipedality of Sahelanthropus tchadensis was hitherto documented at 7 Ma in central Africa (Chad) by cranial evidence. Here, we present the first postcranial evidence of the locomotor behavior of the Chadian hominin with new insights on bipedalism at the early stage of our evolutionary history. The original material was discovered at locality TM 266 (Toros-Menalla fossiliferous area), and consists in one left femur and two antimeric ulnae. These new findings confirm that hominins were already terrestrial biped relatively soon after the human-chimpanzee divergence but also suggest that careful climbing arboreal behaviors was still a significant part of their locomotor repertoire.
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Discoveries in Chad by the Mission Paleoanthropological Franco-Tchadienne (MPFT) have substantially contributed to our understanding of early human evolution in Africa. The locality TM 266 (Extended data 1) in the Toros-Menalla fossiliferous area in the Mega-Chad basin yielded, among hundreds of vertebrate remains, a nearly complete cranium (TM 266-01-60-1), three mandibles, and several isolated teeth depicting a minimum of three adult individuals assigned to Sahelanthropus tchadensis1,2. TM 266 fossils were found in the Anthracotheriid Unit with biochronological estimates and radiochronological age at ca. 7 Ma3,4. Environmental indicators at Toros-Menalla localities, at the time, suggested a lacustrine fringe, in a desert vicinity, where open areas with dry and humid grasslands coexisted with arboreal cover5,6.
Three other hominin fossil remains were discovered at TM 266 in 2001 by the MPFT: one left femoral shaft (TM 266-01-063, unearthed in July 2001), and two right and left ulnae (respectively TM 266-01-358, unearthed in November 2001 and TM 266-01-050, unearthed in July 2001; Supplementary notes). Despite none of these limb bones can be reliably ascribed to any hominin craniodental specimen found at TM 266, the most parsimonious hypothesis is that these postcranial remains belong to the sole hominin species present in this locality. Hence, we favor a conservative attribution of these specimens to Sahelanthropus tchadensis.
The hindlimb is documented by a left femoral shaft (TM 266-01-063) of about 242 mm long (Fig. 1 and Supporting table 1, Extended data 2), lacking the distal epiphysis and most of the proximal one. The specimen is curved anteroposteriorly as in Australopithecus7-9 and Orrorin tugenensis (BAR 1002’00 and BAR 1003’00) but more heavily built. The two major mediolateral axes of the proximal and distal diaphyseal portions clearly indicate that the neck must have been anteverted as in fossil hominins9-11 (Extended data 3). The presence of a groove on the postero-superior surface of the neck for the obturator internus and m. gemelli supports this interpretation. Resulting in head/neck torsion relative to the long axis of the shaft12.This condition is also reported in archaic fossil apes such as Nacholapithecus and Ekembo but is absent in the arboreal biped Danuvius13. The femur exhibits proximal platymeria just distal to the lesser trochanter (Supplementary notes), a trait encountered in O. tugenensis and later hominins and suggested to correlate with neck elongation, a reliable indicator of hominin bipedalism9,14-16 (but see 8,17). Concurrently, the neck is compressed antero-posteriorly as in the Miocene ape Danuvius guggenmosi13 and hominins8-9,18 (but see 19 for Dryopithecus fontani and Hispanopithecus laietanus; Fig. 1). This array of features agrees with habitual bipedalism in S. tchadensis.
A small but sharp relief, indicative of the third trochanter, continues into a rugose surface distally and blends with the lateral component of a broad ‘proto-linea aspera’17 (12.2mm in its narrowest width). The lateral lip of the linea forms a well-marked sigmoid line. Similarly, the medial lip of the linea aspera is well-marked. The spiral line for the insertion of the vastus medialis consists in a straight line, which confounds distally with the medial lip of the linea aspera. Such configuration is also observed in O. tugenensis and Ardipithecus ramidus8,16,18 albeit with a more salient ‘proto-linea aspera’ in TM 266-01-063, but differs from modern humans where a pilaster develops. Such an overall pattern is consistent with bipedalism albeit suggesting a less-developed quadriceps system relative to the hamstring compared to modern human-like pattern17.
The femoral shaft exhibits thick cortical bone in cross-section (Fig. 2). Cortical thickness distribution pattern describes a posterior and lateral thickening of the diaphysis relative to an anterior and medial thinning (Fig. 3). Posterior thickening of the cortical bone occurs at the level of the nutrient foramen, where the ‘proto-linea aspera’ is the narrowest. Conversely, extant apes share a posterior thickening on proximal half of the shaft and a relative thinning on distal half20 (see also Supporting Information in 21). Lateral thickening can be traced on the major part of the shaft in TM 266-01-063 except in its most distal portion. African apes do not display extended lateral thickening but instead, a circumscribed thickening corresponding to the lateral spiral pilaster. In these aspects, TM 266-01-063 most resembles extant humans. Comparative data are, to our knowledge, inexistent for Ardipithecus. Besides, cortical thickness data reported for BAR 1002’00 (O. tugenensis) rely on CT-scan data whose reliability is questionable22-24.
Cortical area and second moment of area (Ix/Iy and Imax/Imin are biomechanical parameters frequently used to infer habitual locomotor functions in primates, as they reflect loads undergone by long bones during growth (but see 25). The cortical area of the diaphyseal cross-section is a measure of resistance of the bone to axial compression or tension, while second moment of area measures the resistance to bending loads. In TM 266-01-063, percent of cortical area is 66.5 % at the level of the nutrient foramen (see Methods) and slightly increase proximally. It is within the range of extant and fossil apes (75 % ± 3.6 in extant humans; 63.3 % ± 7.6 in chimpanzees; 70 % ± 3.9 in gorillas; Supporting Information in 21) and above the value reported for AL 288-1 femur (59.9 %) at midshaft26. Response to bending loads endured by the femur from TM 266 is assessed at the level of the nutrient foramen using second moment of area26,27. Results for Imax/Imin and Ix/Iy are respectively 1.31 and 0.81 (Extended data 4). The Chadian femur approaches the chimpanzee/extant human condition in its Imax/Imin ratio (measured at midshaft28,29; humans, Imax/Imin=1.6 ± 0.36; chimpanzees, Imax/Imin=1.4 ± 0.2) whereas it departs from gorillas28 (Imax/Imin=1.9 ± 0.3). The Ix/Iy of TM 266-01-063 is close to values reported for chimpanzees (chimpanzee30: Ix/Iy=0.75 ± 0.08), early Homo31-33 and early to Middle Pleistocene hominins34. It departs from extant humans in which a posterior pilaster develops29 (Ix/Iy =1.52 ± 0.39). Whereas midshaft cross-section of TM 266-01-063 resembles in its overall aspect to AL 288-1, the Chadian specimen present higher Imax/Imin and lower Ix/Iy values than its younger eastern-African relative (A. afarensis: AL 288-126, Ix/Iy=0.98 and Imax/Imin=1.07; see also 35 for AL 333-61, Ix/Iy=1.16 and Imax/Imin=1.16).
Many aspects such as stature, body mass, muscle attachment sites, positional behavior, ontogeny and sexual dimorphism25 may contribute to femoral bone mass distribution. Yet, geometry of the TM 266-01-063 indicates greatest bending resistance for medio-laterally oriented stresses. This condition seen in AL 288-1 and early African and Asian Homo is suggested to relate to a more lateral position of the body during the stance phase of gait in association with an increase in femoral neck length and biacetabular breadth26. Functional interpretations remain difficult to formulate given the paucity of early hominin comparative data and given the state of preservation of the Chadian femur. Nevertheless, the Chadian femoral shaft exhibits a well-developed calcar femorale (CF) in its proximal portion (Fig. 4; the CF is 18.80 mm long measured at the level of the lesser trochanter following36), a condition to date only seen in extant humans and reported in O. tugenensis (BAR 1003’00). The calcar femorale corresponds to a bony wall that originates from the postero-medial endosteal surface at the level of the lesser trochanter and extends laterally toward the greater trochanter. In obligate bipeds, it facilitates compressive loads dispelling in the proximal femur by decreasing the stress in the posterior and medial aspects and increasing the stress in the anterior and lateral aspects36,37. A well-developed calcar femorale in TM 266-01-063 represents a morphological requirement for terrestrial bipedalism.
The forearm bones attributed to Sahelanthropus tchadensis consist in two partial left and right ulnae lacking the distal epiphyses. Similarity in size and shape for the antimeric ulnae could suggest they are from the same individual, even if no definitive evidence supports this assumption. TM 266-01-050 is a left ulnar diaphysis of 239 mm long (Fig. 5, Supporting table 1, Extended data 2) showing eroded proximal epiphysis. The right ulna (TM 266-01-358) corresponds to a proximal-half shaft of 155 mm long with partially preserved epiphysis. The shafts are curved in profile. Similar anteroposterior curvature is observed in Ar. kadabba38 (ALA-VP 2/101) and later hominins StW 573k and OH 36, as in extant apes9,39,40. This feature contrasts with the straight right ulnar shafts of D. guggenmosi and A. prometheus, but this lack of curvature is likely due to a pathological condition9,13. In primates, such ulnar curvature is due to habitual loads exerted by the action of m. brachialis in order to maintain elbow flexion in arboreal context, which in turn involves the antagonistic action of a powerful forearm musculature, including wrist and fingers extensors and flexors40,41.
The preserved flat distal portion of the olecranons indicate that they were not projecting posteriorly as in extant African apes42. In this regard, the distal portion of the olecranon most resembles the condition seen in Miocene apes42-44 and in hominins42. The proximal epiphyses indicates an anteriorly-facing trochlear notch as in fossil hominins and Miocene apes9,13,42-45. Hence, the Toros-Menalla ulnae depart from the typical proximally oriented trochlear notch in extant great apes41,46. In functional terms, a more anteriorly facing notch, associated with an olecranon aligned with the long axis of the forearm, favors triceps leverage at mid-flexion41,46. In Ar. ramidus such function is linked to careful climbing and bridging44. Conversely, a more proximally facing notch reflects differential loading during suspension43 while a posteriorly projecting olecranon favors triceps leverage in extension and is commonly associated with terrestrial quadrupedal locomotion in anthropoids42.
Ulnae from Toros-Menalla display a keeled trochlear notch with a comparatively acute angle relative to later hominins and African apes. The distal keeling angle, measured from TM 266-01-358 (distal keeling angle=109°), is in the lower range of Pongo pygmaeus and close to the value reported for Oreopithecus bambolii and the left ulna AL 288-1t in A. afarensis46. Likewise, the proximal angle is acute (proximal keeling angle=100°), in the lower range of reported values for chimpanzees, and close to OH 36 and Or. bambolii46. A pronounced trochlear keel warrants medio-lateral stability of the elbow in response to powerful superficial finger and wrist flexors, and forearm pronator (mm flexor digitorum superficialis, flexor carpi radialis and ulnaris, and pronator teres)39,46. Such configuration was supposedly reported on D. guggenmosi13 and is typical of the arboreal large apes, which integrates climbing, and/or suspension in their locomotor repertoire46. It is unlikely to reflect habitual terrestrial quadrupedalism. The TM 266 ulnae lack prominent flexor apparatus entheses as in orangutans, Ar. ramidus and later hominins. In this respect, it differs from the condition seen in Miocene apes and extant quadrupedal monkeys. Such morphology precludes the possibility of quadrupedalism and, more specifically, of knuckle-walking as primary locomotor behaviors for the Toros-Menalla hominins45.
Overall, the trochlear notch of TM 266 ulnae present an unusual morphology as the middle portion is mediolaterally narrow relative to the distal half. This waisted aspect of the trochlear notch approaches the condition seen in ‘small’ apes (humans, chimpanzees and bonobos) and contrasts with that of ‘large’ apes (orangutans and gorillas). Such configuration is interpreted as locomotor-independent and rather linked to allometry46. The disto-medial quadrant of TM 266-01-358 is clearly more developed than the distolateral one, an intermediate morphology between humans and chimpanzees, close to that of D. guggenmosi13, A. afarensis, and A. prometheus 9,46. A developed medial portion of the trochlear notch is an adaptation for maximum joint compression medially, a configuration which could meet mechanical requirements in various non terrestrial locomotor behaviors13,46.
Only limited portions, proximally and distally, of TM 266-01-050 allow assessing cortical bone distribution (see Supplementary notes, Extended data 4). Proximally, the percent of cortical area is 73.4 %, measured at about 70-75 % of the estimated total lengths of the ulna (see methods). At mid-shaft, the percent of cortical area is 81.0 %, falling within the variation of Late Pleistocene hominins (80.1 % ± 6.6 in H. sapiens and 82.8 % ± 7.1 in neandertals)47. Besides, Imax/Imin and Ix/Iy are respectively 2.04/1.62 at 70-75 % level and 1.71/1.13 at midshaft. Values for the Chadian ulna fall outside the reported variation for gorillas48 and is within the range of variation in chimpanzees for proximal Imax/Imin and proximal-midshaft Ix/Iy. Besides, TM 266-01-050 is within the range of variation of Asian non-human apes for all ratios except for the lower measured proximal Imax/Imin in Pongo. The geometry of TM 266-01-050 deviates from circularity in the antero-posterior direction. The cortical bone is predominantly distributed antero-posteriorly as in orangutans and to a lesser extent in chimpanzees. This condition contrasts with the one seen in gorillas, which tend to grow more bone medio-laterally. Relative medio-lateral expansion is suggested to adjust for increased vertical and medio-lateral forces that apply to the forelimb in terrestrial quadrupedal primates45,49,50. Besides, considering comparative data available for chimpanzees and orangutans, which tend to grow more bone antero-posteriorly51, the Chadian ulna configuration more likely reflects bending loads associated with a wide array of arboreal locomotor modes. Yet, the TM forelimb bones lack any traits typical of suspension or knuckle walking, and exhibit a configuration better seen in apes engaged in careful climbing44. However, the possibility that the Chadian hominin was capable of vertical climbing cannot be dismissed given the particularly keeled trochlear notch.
The Toros-Menalla femur exhibits several hallmarks of habitual terrestrial bipedalism. Among them, a well-defined broad proto-linea aspera, the presence of a lateral third trochanter and associated subtrochanteric platymeria without hypotrochanteric or infero-lateral fossae, is classically associated with enhanced hip flexion-extension16,20,52, while a particularly developed calcar femorale facilitates compressive loads dispelling in terrestrial bipedalism36. These features go with an overall cortical bone distribution pattern and cross-section geometries of the femoral shaft that suggest muscular recruitments and bone loads compatibles with habitual bipedalism. Despite some of the above-mentioned traits are suggested to be the primitive condition in hominins (proximal platymeria or gluteal tuberosity)17, they are part of a functional complex co-opted for bipedalism. They are routinely considered as such to infer potential bipedal terrestrial locomotion in early eastern African hominins7,8,16,18,52,53. The Chadian hindlimb bone conforms to the overall morphological pattern of Miocene hominin terrestrial bipeds. The forelimbs morphology rules out arboreal specialization for the Chadian material, as in Ar. ramidus16 and presumably O. tugenensis7. Yet, the Chadian postcranial material displays a suite of morphological features that are consistent with substantial non-stereotypical arboreal behaviors, as suggested by ulnar shaft curvature and cross-section geometrical properties, whereas the elbow morphology is potentially indicative of careful climbing44, and does not display any evidence of knuckle-walking.
Recently, it was suggested that the putative stem hominid D. guggenmosi was able to use obligate arboreal bipedalism combined to suspension as early as the late middle Miocene13. The authors suggested that hominin terrestrial bipedalism and great ape suspension evolved from such locomotor repertoire13. In the lack of evidence supporting a phylogenetic relationship between hominins and Miocene European apes, we cannot infer that hominin terrestrial bipedalism originated from middle Miocene forms in Europe as suggested by 13. Instead, the Chadian remains described herein reassert African roots. They are the first direct evidence of an obligate terrestrial bipedalism, indistinguishable from that inferred for O. tugenensis and Ar. kadabba/ramidus. They suggest a precocious adaptation to bipedalism after the human-chimp dichotomy54. The Chadian remains suggests a conservative evolution of climbing capacities, interpreted as cautious climbing as in stem apes54. Hence, cautious climbing modality weakens a potential role of suspension in the emergence of the hominin clade13.
The Toros-Menalla postcranial material also reasserts the presence of cladistic hominins in the upper Miocene of Chad, within particular environmental settings. Eastern African Miocene hominins are associated with open woodland areas with significant tree cover at ~6 Ma at Lukeino55, and a mixture of woodland combined with wet grassland for the earliest postcranial-based bipedalism occurrence in Ethiopia at 5.2 Ma (AME-VP-1/71, Ardipithecus kadabba)38,56. At 4.4 Ma, Ar. ramidus most probably inhabited a ground-water-fed grassy woodland (probably a palm grove) at Aramis57-58.
Taken as a whole, eastern-African early hominins share an arboreal component in their habitat (see 57,59 for discussion on Aramis). Environmental indicators in Toros-Menalla fossiliferous area suggest heterogeneous landscape types consisting of closed forest formations (probably riparian forests), palm grove formations, and mixed/grassland formations (from woodlands to savannas/aquatic grasslands)5,6,60. Therefore, the Chadian hominins were probably no exception as being reliant on arboreal cover given their potential climbing abilities. As bipeds, they were not exclusive arboreal forest dwellers, because they were able to raid in near open environments for food/water resource harvesting. The association between a polyvalent locomotion (arboreality and bipedal terrestriality), and wooded formations in mesic context during at least ~2.5 million years suggests that the ecological niche of these early hominins was not strongly tied to the expansion of relatively dry, open areas. This niche could be depicted as opportunistic in its reliance on both terrestrial and arboreal resources.
Based on molecular data, the chimpanzee-human last common ancestor (CHCLA) is estimated to occur in Africa between 10 and 7 Ma61,62. Indeed, fossil representatives of the panin clade are too scarce and consists in a minimum of three Middle Pleistocene teeth from the Kapthurin formation in Kenya63 and a chimpanzee-like proximal femoral epiphysis of unknown age from the Kikorongo crater in Uganda64. However, at least three taxa have been described between 10 Ma and 7 Ma in African deposits: Samburupithecus, from Samburu Hills, around 9.5 Ma65, Nakalipithecus from Nakali, around 9,8 Ma66 and Chororapithecus from the Middle Awash, around 8 Ma62,67. These Miocene taxa are parsimoniously assigned to stem hominines68,69, even if Samburupithecus displays a particularly archaic morphology69. Chororapithecus displays derived dental affinities with Gorilla67. In light of this record and of the lack of phylogenetic resolution, the ancestral condition of positional behaviour in African apes and humans will remain elusive until significant new data becomes available. To date, the identification of the derived traits shared by hominins relies on the analysis of the earliest forms of the clade. The early hominins Sahelanthropus, Orrorin and Ardipithecus share the same combination of non-honing C-P3 complex and of features linked to terrestrial bipedalism. This combination is arguably more similar to the condition observed in later hominins than in any other African fossil or extant hominoids. This is currently the only data available for formulating scenarios about the latest Miocene/earliest Pliocene evolution of African hominoids. In absence of Mio-Pliocene fossils displaying exclusive morphological affinities with Pan, cautionary tales about rampant homoplasy and character polarity in this evolutionary sequence70 are poorly suitable to falsification attempts. Instead, the morphological homogeneity of the purported hominids implies that the interpretation of the combined non-honing C-P3 complex-bipedal hindlimb as a synapomorphic signature of early hominids currently remains the most parsimonious hypothesis
The original fossil specimens are measured to the nearest 0.1 mm using a Mitutoyo sliding digital caliper.
Computed tomography
High-resolution micro-computed tomography (HR-mCT) images taken from the original femur and ulnae were used to assess the inner morphology of the bones. The material was scanned with EasyTom XL Duo mCT (using a sealed Hamamatsu microfocus x-ray source - 75 W, 150 kV - and an amorphous silicon based detector Varian PaxScan 2520DX, 1536*1920 pixel matrix; 127 mm pixel pitch, 16 bits, CsI conversion screen - from RX-Solutions, France) at Plateforme PLATINA (University of Poitiers). For scanning procedures, beam intensity was set at 90 kV and tube current at 333 mA. The TM 266- 01-358 ulna was acquired with 3584 projections resulting in 3036 slices of 730*825 pixels using a cone-beam reconstruction algorithm. The isovoxel size was set to 0.0525 mm. The TM 266-01-050 ulna was acquired with 4800 projections resulting in 4051 slices of 589*849 pixels. The isovoxel size was set to 0.0600 mm. The TM 266-01-063 femur was acquired with 5984 projections resulting in 4962 slices of 1162*911 pixels. The isovoxel size was set to 0.0499 mm.
Virtual models processing
Semi-automatic segmentation of the virtual fossil specimens and three-dimensional surfaces extraction were performed in Avizo Lite. Three-dimensional surfaces were prepared and treated using Geomagic Studio. Cortical bone thickness distribution was assessed in three dimensions using the Surface thickness module in Avizo Lite from the outer surface of the of the segmented medullar cavity to the outer surface of the femur. All measurements based on 3D virtual models of the fossil specimen were done in Avizo Lite on 3D volumes and Fiji image software71 on 2D slices.
Cross-sectional geometric properties (CSGP)
The femur lacks the most part of the epiphyses, which prevents from estimating its biomechanical length. However, CSGP values in Homo and Pan do no show significant differences between 45-55 % of the femoral (biomechanical or maximum) length31. Comparison of diaphyseal cross-sectional geometry from fragmentary specimens must be evaluated on a case-by-case basis31. Superimposition of the femora BAR 1002'00 (O. tugenensis) and TM 266-01-063 using the distal base of their lesser trochanter (corresponding to 80 % of the biomechanical length72), show that the nutrient foramen on TM 266-01-063 provides a reliable indicator of the midshaft level. CSGP estimates were computed at nutrient foramen level and then, in order to get an assessment of the variation pattern of cortical bone distribution, at four additional cross-sections, equally spaced from the nutrient foramen to the base of the lesser trochanter. For ulnae, CSGP variables were computed proximally from 35.0 mm below the distal border of the radial notch (and at the level of the nutrient foramen), which corresponds to 70-75 % of the estimated ulna length for TM 266-01-050 (estimated using OMO L40-19 fossil hominin ulna as analog).
Percentage of cortical area and second moment of area were computed using Fiji image software71 and BoneJ plugin73.
Comparative data for CSGP with extant and extinct hominoids (Extended data 4) were gathered from 19,21,26,28-30,32,33,35,74,75.
- Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nature methods 9, 676-682 (2012).
- Ruff, C. B. Long bone articular and diaphyseal structure in Old World monkeys and apes. I: locomotor effects. Am. J. Phys. Anthrop. 119, 305-342 (2002)
- 73. Doube, M. et al. BoneJ: Free and extensible bone image analysis in ImageJ. Bone 47, 1076-1079 (2010).
- MaClatchy, L., Gebo, D., Kityo, R., & Pilbeam, D. Postcranial functional morphology of Morotopithecus bishopi, with implications for the evolution of modern ape locomotion. J. Hum. Evol. 39, 159-183 (2000).
- Rodríguez, L., Carretero, J. M., García-González, R., & Arsuaga, J. L. Cross-sectional properties of the lower limb long bones in the Middle Pleistocene Sima de los Huesos sample (Sierra de Atapuerca, Spain). J. Hum. Evol. 117, 1-12 (2018).
Author contributions
G.D. and F. G. designed the study, collected and interpreted the data. G.D., F.G. and J.-R. B. wrote the manuscript. G. D., F. G., J.-R. B., M.H.T., A.L., M.A., P.V. and C.N. discussed the results and revised earlier drafts of the papers.
Acknowledgments
We thank the Chadian Authorities (Ministère de l’Education Nationale de l’Enseignement Supérieur, de la Recherche et de l’Innovation, Université de Djamena & CNRD). We extend gratitude for their support to the French Ministries, Ministère Français de l’Education Nationale (Collège de France, Université de Poitiers), Ministère de la Recherche (CNRS), Ministère de l’Europe et des affaires étrangères (Direction de la Coopération Scientifique, Universitaire et de Recherche, Paris, and SCAC Ambassade de France à N’djamena, Commission de Consultation des recherches Archéologiques à l'Etranger), to the Région Nouvelle Aquitaine, and also to the Armée Française (MAM, Epervier and Barkhane) for logistic support. We would like to thank deeply to Professor M. Brunet, head of the M.P.F.T., who initiated this work and gathered the first comparative data at the basis of the present manuscript. For giving him the opportunity to work with their collections, we are grateful to our Colleagues and their Institutions: C.O. Lovejoy (Kent State University), B. Asfaw (National Museum of Ethiopia), Y. Haile-Selassie (Cleveland Museum of Natural History), M. G. Leakey & R. Leakey (National Museum of Kenya), D. Pilbeam (Peabody Museum and Harvard University), D. Johanson & W. Kimbel (Institute of Human Origins and Arizona State University at Tempe), T. White (University of California at Berkeley) and G. Suwa (University Museum of Tokyo). Special thanks to all our colleagues and friends for their help and discussion, and particularly to D. Barboni, A. Mazurier (Centre de Microtomographie), A. Novello. We especially thank all the MPFT members who participated to the field missions, and Ahounta D., Fanoné G. (deceased), Mahamat A., S. Riffaut, J. Surault and X. Valentin for technical support. We are most grateful to G. Florent, C. Noël, G. Reynaud, C. Baron, M. Pourade, and L. Painault for administrative guidance.
- Brunet, M. et al. A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418, 145–151 (2002).
- Brunet, M. et al. New material of the earliest hominid from the Upper Miocene of Chad. Nature 434, 752–755 (2005).
- Vignaud, P. et al. Geology and palaeontology of the Upper Miocene Toros-Menalla hominid locality, Chad. Nature 418, 152–155 (2002).
- Lebatard, A. E. et al. Cosmogenic nuclide dating of Sahelanthropus tchadensis and Australopithecus bahrelghazali: Mio-Pliocene hominids from Chad. Proc. Natl. Acad. Sci. USA 105, 3226–3231 (2008).
- Le Fur, S., Fara, E., Mackaye, H. T., Vignaud, P., & Brunet, M. The mammal assemblage of the hominid site TM266 (Late Miocene, Chad Basin): ecological structure and paleoenvironmental implications. Naturwissenschaften 96, 565–574 (2009).
- Schuster, M. et al. Chad Basin: paleoenvironments of the Sahara since the Late Miocene. C. R. Geosci. 341, 603–611 (2009).
- Senut, B. et al. First hominid from the Miocene (Lukeino formation, Kenya). C. R. Acad. Sci. Paris IIA 332, 137–144 (2001).
- Pickford, M., Senut, B., Gommery, D., & Treil, J. Bipedalism in Orrorin tugenensis revealed by its femora. C. R. Palevol 1, 191–203 (2002).
- Heaton, J. L. et al. The long limb bones of the StW 573 Australopithecus skeleton from Sterkfontein Member 2: Descriptions and proportions. J. Hum. Evol. 133, 167–197 (2019).
- Lovejoy, C. O., Cohn, M. J., & White, T. D. Morphological analysis of the mammalian postcranium: a developmental perspective. PNAS, 96, 13247–13252 (1999).
- Tardieu, C. Development of the human hind limb and its importance for the evolution of bipedalism. Evol Anthrop: Issues, News, and Reviews, 19, 174–186 (2010).
- Marchi, D. et al. The thigh and leg of Homo naledi. J. Hum. Evol. 104, 174–204 (2017).
- Böhme, M. et al. A new Miocene ape and locomotion in the ancestor of great apes and humans. Nature, 575, 489–493 (2019).
- Ruff, C. in Primate Locomotion: Recent Advances (eds. Strasser, E., Fleagle, J., Rosenberger, A.L., & McHenry, H.) 449–469 (Springer, Boston, MA, 1998).
- Lovejoy, C. O., Meindl, R. S., Ohman, J. C., Heiple, K. G., & White, T. D. The Maka femur and its bearing on the antiquity of human walking: applying contemporary concepts of morphogenesis to the human fossil record. Am. J. Phys. Anthropol. 119, 97–133 (2002).
- Lovejoy, C. O., Suwa, G., Spurlock, L., Asfaw, B., & White, T. D. The pelvis and femur of Ardipithecus ramidus: the emergence of upright walking. Science 326, 71e1-71e6 (2009).
- Almécija, S. et al. The femur of Orrorin tugenensis exhibits morphometric affinities with both Miocene apes and later hominins. Nat. Commun. 4, 2888 (2013).
- Richmond, B. G., & Jungers, W. L. Orrorin tugenensis femoral morphology and the evolution of hominin bipedalism. Science 319, 1662–1665 (2008).
- Pina, M. Unravelling the positional behaviour of fossil hominoids morphofunctional and structural analysis of the primate hindlimb. Doctoral dissertation, Universitat Autònoma de Barcelona (2016).
- Morimoto, N., De León, M. S. P., Nishimura, T., & Zollikofer, C. P. Femoral morphology and femoropelvic musculoskeletal anatomy of humans and great apes: a comparative virtopsy study. Anat. Rec. 294, 1433–1445 (2011).
- Macchiarelli, R. & Zanolli, C. Hominin biomechanics, virtual anatomy and inner structural morphology: From head to toe. A tribute to Laurent Puymerail. C. R. Palevol 16, 493–498 (2017).
- Eckhardt, R. B., Galik, G., & Kuperavage, A. J. Questions about Orrorin femur: response. Science 307, 845 (2005).
- Galik, K. et al. External and internal morphology of the BAR 1002'00 Orrorin tugenensis femur. Science 305, 1450–1453 (2004).
- Ohman, J. C., Lovejoy, C. O., & White, T. D. Questions about Orrorin femur. Science 307, 845 (2005).
- Lieberman, D. E., Polk, J. D., & Demes, B. Predicting long bone loading from cross-sectional geometry. Am. J. Phys. Anthropol. 123, 156–171 (2004).
- Ruff, C. B., Burgess, M. L., Ketcham, R. A., & Kappelman, J. Limb Bone Structural Proportions and Locomotor Behavior in AL 288-1 (" Lucy"). PLoS ONE 11, e0166095 (2016).
- Lovejoy, C. O., Burstein, A. H., & Heiple, K. G. The biomechanical analysis of bone strength: a method and its application to platycnemia. Am. J. Phys. Anthropol. 44, 489–505 (1976).
- Mongle, C. S., Wallace, I. J. & Grine, F. E. Cross-sectional structural variation relative to midshaft along hominine diaphyses. II. The hind limb. Am. J. Phys. Anthropol. 158, 398–407 (2015).
- Trinkaus, E. & Ruff, C. B. Femoral and Tibial Diaphyseal Cross-Sectional Geometry in Pleistocene Homo. PaleoAnthropology 2012, 13–62 (2012).
- Nadell, J. Ontogeny and Adaptation: A Cross-Sectional Study of Primate Limb Elements. Doctoral dissertation, Durham University (2017).
- Puymerail, L. et al. Structural analysis of the Kresna 11 Homo erectus femoral shaft (Sangiran, Java). J. Hum. Evol. 63, 741–749 (2012).
- Ruff, C. Femoral/humeral strength in early African Homo erectus. J. Hum. Evol. 54, 383–390 (2008).
- Ruff, C. Relative limb strength and locomotion in Homo habilis. Am. J. Phys. Anthropol. 138, 90–100 (2009).
- Ruff, C. B., Puymerail, L., Macchiarelli, R., Sipla, J., & Ciochon, R. L. Structure and composition of the Trinil femora: functional and taxonomic implications. J. Hum. Evol. 80, 147–158 (2015).
- Chevalier, T. AL 333 – 61 femoral diaphysis: evidence of obligate bipedalism 3.2 million years ago in Ethiopia? Bull. Mém. Soc. Anthropol. Paris 25:169–189 (2013).
- Kuperavage, A., Pokrajac, D., Chavanaves, S. & Eckhardt, R. B. Earliest known hominin calcar femorale in Orrorin tugenensis provides further internal anatomical evidence for origin of human bipedal locomotion. Anat. Rec. 301, 1834–1839 (2018).
- Zhang, Q. et al. The role of the calcar femorale in stress distribution in the proximal femur. Orthop. surg., 1, 311–316 (2009).
- Haile-Selassie, Y., Suwa, G. & White, T. in Ardipithecus kadabba: Late Miocene Evidence From The Middle Awash, Ethiopia (eds. Haile-Selassie, Y., & WoldeGabriel, G.) 159–236 (Univ of California Press, 2009).
- Drapeau, M. S. M., Ward, C. V., Kimbel, W. H., Johanson, D. C., & Rak, Y. Associated cranial and forelimb remains attributed to Australopithecus afarensis from Hadar, Ethiopia. J. Hum. Evol. 48, 593–642 (2005).
- Henderson, K., Pantinople, J., McCabe, K., Richards, H. L. & Milne, N. Forelimb bone curvature in terrestrial and arboreal mammals. PeerJ 5, e3229 (2017).
- Drapeau, M. S. M. Functional anatomy of the olecranon process in hominoids and Plio-Pleistocene hominins. Am. J. Phys. Anthropol. 124, 297–314 (2004).
- Begun, D. R. Phyletic diversity and locomotion in primitive European hominids. Am. J. Phys. Anthropol. 87, 311–340 (1992).
- Takano, T. et al. Forelimb long bones of Nacholapithecus (KNM-BG 35250) from the middle Miocene in Nachola, northern Kenya. Anthropol. Sci. 126, 135–149 (2018).
- Lovejoy, C. O., Simpson, S. W., White, T. D., Asfaw, B., & Suwa, G. Careful climbing in the Miocene: the forelimbs of Ardipithecus ramidus and humans are primitive. Science 326, 70e1-70e8 (2009).
- Alba, D. M., Almécija, S., Casanovas-Vilar, I., Méndez, J. M., & Moyà-Solà, S. A partial skeleton of the fossil great ape Hispanopithecus laietanus from Can Feu and the mosaic evolution of crown-hominoid positional behaviors. PLoS ONE 7, e39617 (2012).
- Drapeau, M. S. M. Articular morphology of the proximal ulna in extant and fossil hominoids and hominins. J. Hum. Evol. 55, 86–102 (2008).
- Churchill, S. E. et al. Morphological affinities of the proximal ulna from Klasies River main site: archaic or modern? J. Hum. Evol. 31, 213–237 (1996).
- Nadell, J.A. Ontogeny and adaptation: a cross-sectional study of primate limb elements, Doctoral dissertation, Durham University (2017).
- Carlson, K.J. et al. Role of nonbehavioral factors in adjusting long bone diaphyseal structure in free-ranging Pan troglodytes. Int. J. Primatol. 29, 1401–1420 (2008).
- Schmitt, D. Mediolateral reaction forces and forelimb anatomy in quadrupedal primates: implications for interpreting locomotor behavior in fossil primates. J. Hum. Evol. 44, 47–58 (2003).
- Morimoto, N. et al. Let bone and muscle talk together: a study of real and virtual dissection and its implications for femoral musculoskeletal structure of chimpanzees. J. Anat. 226, 258–267 (2015).
- White, T. D. et al. Asa Issie, Aramis and the origin of Australopithecus. Nature 440, 883–889 (2006).
- Ward, C. V., Kimbel, W. H., Harmon, E. H. & Johanson, D. C. New postcranial fossils of Australopithecus afarensis from Hadar, Ethiopia (1990–2007). J. Hum. Evol. 63, 1–51 (2012).
- Lovejoy, C. O. et al. The great divides: Ardipithecus ramidus reveals the postcrania of our last common ancestors with African apes. Science 326, 73–106 (2009).
- Bamford, M. K., Senut, B. & Pickford, M. Fossil leaves from Lukeino, a 6-million-year-old Formation in the Baringo Basin, Kenya. Geobios 46, 253–272 (2013).
- WoldeGabriel, G. et al. Geology and palaeontology of the late Miocene Middle Awash valley, Afar rift, Ethiopia. Nature 412, 175–178 (2001).
- White, T. D. et al. Macrovertebrate paleontology and the Pliocene habitat of Ardipithecus ramidus. Science 326, 67–93 (2009).
- Barboni, D., Ashley, G. M., Bourel, B., Arraiz, H. & Mazur, J. C. Springs, palm groves, and the record of early hominins in Africa. Rev. Palaeobot. Palynol. 266, 23–41 (2019).
- Cerling, T. E. et al. Woody cover and hominin environments in the past 6 million years. Nature 476, 51–56 (2011).
- Novello, A. et al. Phytoliths indicate significant arboreal cover at Sahelanthropus type locality TM266 in northern Chad and a decrease in later sites. J. Hum. Evol. 106, 66–83 (2017).
- Steiper, M. E. & Young, N. M. Timing primate evolution: lessons from the discordance between molecular and paleontological estimates. Evol. Anthropol. 17, 179–188 (2008).
- Katoh, S. et al. New geological and palaeontological age constraint for the gorilla–human lineage split. Nature 530, 215–218 (2016).
- McBrearty, S. & Jablonski, N. G. First fossil chimpanzee. Nature 437, 105–108 (2005).
- DeSilva, J., Shoreman, E. & MacLatchy, L. A fossil hominoid proximal femur from Kikorongo Crater, southwestern Uganda. J. Hum. Evol. 50, 687–695 (2006).
- Ishida H. & Pickford M. A new late Miocene hominoid from Kenya: Samburupithecus kiptalami gen. et sp. nov. C.R. Acad. Sci. Paris 325,823–829 (1997).
- Kunimatsu, Y. et al. A new Late Miocene great ape from Kenya and its implications for the origins of African great apes and humans. Proc. Natl Acad. Sci. USA 104, 19220–19225 (2007).
- Suwa G., Kono R.T., Katoh S., Asfaw B. & Beyene Y. A new species of great ape from the late Miocene epoch in Ethiopia. Nature 448, 921–924 (2007).
- Harrison, T. in Cenozoic Mammals of Africa (eds. Werdelin, L. & Sanders,W.J.) 429–469 (Univ of California Press, Berkeley, 2010).
- Begun, D.R. in Handbook of Paleoanthropology, (eds. Henke, W. & Tattersall, I.) 1261–1332 (Springer-Verlag, Berlin Heidelberg, 2015)
- Wood, B. & Harrison, T. The evolutionary context of the first hominins. Nature 470: 347–352 (2011).